Textbook of Stereotactic and Functional Neurosurgery (2nd Edition, Vol.s 1 & 2)

Textbook of Stereotactic and Functional Neurosurgery

Andres M. Lozano, Philip L. Gildenberg, Ronald R. Tasker (Eds.)

Textbook of Stereotactic and Functional Neurosurgery With 1088 Figures and 232 Tables

Editors: Andres M. Lozano Professor of Surgery and RR Tasker Chair in Functional Neurosurgery University of Toronto Senior Scientist, Toronto Western Research Institute President, World Society for Stereotactic and Functional Neurosurgery Canadian Research Chair in Neuroscience (Tier 1) 399 Bathurst St. WW 4-447 Toronto, Ontario M5T 2S8 Canada [email protected] Philip L. Gildenberg Houston Stereotactic Concepts, Inc. 2260 West Holcombe Boulevard Suite 309 Houston, Texas 77030 USA [email protected] Ronald R. Tasker University of Toronto 399 Bathurst St. WW 4-447 Toronto, Ontario M5T 2S8 Canada A C.I.P. Catalog record for this book is available from the Library of Congress ISBN: 978-3-540-69959-0 This publication is available also as: Electronic publication under ISBN 978-3-540-69960-6 and Print and electronic bundle under ISBN 978-3-540-70779-0 This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in other ways, and storage in data banks. Duplication of this publication or parts thereof is only permitted under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permission for use must always be obtained from Springer‐Verlag. Violations are liable for prosecution under the German Copyright Law. ß Springer‐Verlag Berlin Heidelberg 2009 The use of registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Product liability: The publishers cannot guarantee the accuracy of any information about the application of operative techniques and medications contained in this book. In every individual case the user must check such information by consulting the relevant literature. Springer is part of Springer Science+Business Media springer.com Publishing Editor: Gabriele Schro¨der MRW Editor: Sandra Fabiani Printed on acid‐free paper

SPIN: 11534778

2109 – 5 4 3 2 1 0

Andres Lozano dedicates this work To Marie, Alexander and Christopher

Philip L. Gildenberg, MD, PhD, dedicates this ‘‘Textbook of Stereotactic and Functional Neurosurgery’’ to Patricia Franklin Gildenberg, who has been a significant collaborator in everything he has written since 1973. Her contributions and dedication to both the American and World Societies for Stereotactic and Functional Neurosurgery have been important in maintaining the integrity of those organizations throughout the years.

I would like to dedicate my contribution to this book to my late wife, Mary Morris Craig Tasker, who made my career possible. Ronald R. Tasker OC, MD, FRCSC

Preface

This second edition of the Textbook of Stereotactic and Functional Neurosurgery appears just 11 years after the first. The first edition of the Textbook marked the 50th anniversary of the birth of human stereotactic neurosurgery. After an initial period of rapid growth, the field became quiescent in the 1960s when treatment of Parkinson’s disease migrated from stereotactic surgery to medication, primarily L-dopa. When it became apparent that L-dopa was not the final answer to the management of Parkinson’S disease, human stereotaxis had a rebirth, and the first edition followed a few years later. Many patients returned once again to surgical management in the early 1990s, so many neurosurgeons returned to the fields of stereotactic and functional neurosurgery. In the meantime, computer science and imaging techniques had advanced to foster the development of frameless image guided surgery, as well as stereotactic radiosurgery. Consequently, many neurosurgeons were becoming involved with stereotactic surgery, either returning to the field or being introduced to it for the first time. Both groups needed a comprehensive review of the then-current state of the field which was provided by the first edition of the Textbook of Stereotactic and Functional Neurosurgery. During the past 11 years there have been additional significant advances in this field. Computers have advanced to the point where exotic complex surgical programs have become commonplace and computers have become commonly used in the operating room, both for image guidance and physiological verification of targets. Image guided surgery is being used by most neurosurgeons, many of whom may not have had a prior background in stereotactic surgery. Deep brain stimulation for the treatment of motor disorders has become technically feasible and is commonly practiced at many stereotactic centers, using some techniques that were still under development a decade ago and technically advanced stimulating devices. Radiosurgical techniques involve more complex dosimetry than was available earlier, again because of advances in computer technology. Many new possibilities are being opened for both neurosurgical guidance and functional surgery involving targets that had not previously been recognized. These advances have proceeded so rapidly and broadly across several scientific fields that we have a need for a new edition of the Textbook of Stereotactic and Functional Neurosurgery. It is meant to provide a broad background for neurosurgeons, neurologists, and radiation oncologists, radiation physicists, and other scientists in the ever expanding fields of stereotactic neurosurgery, functional neurosurgery, and stereotactic radiosurgery. These fields have become so broad that no other publication covers the information necessary for all those specialists in a single reference source. This book will provide an update on the significant advances, information, and knowledge that have developed during this past decade has and have been scattered through the literature of these disparate specialties. The first edition was edited by Philip L. Gildenberg and Ronald Tasker. Both those stereotactic neurosurgeons retired from active clinical practice in the past 10 years, so they recruited Andres Lozano to be the primary editor. They felt that he brings to this position a unique combination of clinical #

Springer-Verlag Berlin/Heidelberg 2009

xii

Preface

expertise, extensive knowledge of background laboratory information, a record of providing innovation to functional neurosurgery, and has provided leadership for a new generation of stereotactic neurosurgeons. The editors wish to thank McGraw-Hill, who published the first edition, for relinquishing the copyright to Dr. Gildenberg, which opened the door for Springer to publish the second edition. The difference in the editorial process between the first edition and the second edition in some ways reflects the development of computers during that time, and consequently the advances in the fields of stereotactic and functional neurosurgery. The authors who contributed to the first edition sent hard copy printed manuscripts to the editors who would then read for content and copy edit, a timeconsuming and inefficient process. Manuscripts were then mailed back to the authors for final approval and/or correction and sent back to the Editors, possibly several times, who relayed them to the publisher when they were perfected. All manuscript preparation and submission for the second edition were done electronically, so no paper changed hands, which sometimes introduced new complexities, but ultimately proved more efficient, not to mention friendly to the environment. It is noteworthy that between the time of the first edition and the second edition, the operating room also became digitized, with consequent improvement in the display of diagnostic studies, processing information from those studies, and integrating that information into the surgical plan. The editors thank Garbiele Schro¨der and Stephanie Benko of Springer, who made this Textbook possible. The editors especially wish to thank Andrew Spencer and his staff at Springer, who served as the publisher’s representative to this project and maintained the flow of digital information between authors, editors and publisher. The editors also wish to thank Joan Richardson, who served as a liaison between the authors, editors, and publisher’s staff, and provided an accurate update on the progress and problems of each chapter and author. She managed the organization of 195 manuscripts with over 250 authors, with occasional changes in authors or topics, to facilitate communication between the editors and authors.

Table of Contents

Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xi Contributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xxix

Section 1 History of Stereotactic Surgery . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 1 History of Stereotactic Surgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 P. L. Gildenberg . J. K. Krauss

2 History of the Stereotactic Societies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35 P. L. Gildenberg . J. K. Krauss

3 History of Stereotactic Surgery in US . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45 P. L. Gildenberg

4 History of Stereotactic Surgery in Germany . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53 J. K. Krauss

5 History of Stereotactic Surgery in Japan . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59 C. Ohye

6 History of Stereotactic Neurosurgery in the Nordic Countries . . . . . . . . . . . . . . . . . . 65 B. A. Meyerson . B. Linderoth

7 A Brief History of Stereotactic Neurosurgery in Switzerland . . . . . . . . . . . . . . . . . . . 73 E. Taub

8 History of Stereotactic Surgery in Great Britain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77 E. A. C. Pereira . A. L. Green . D. Nandi . T. Z. Aziz

9 History of Stereotactic Surgery in France . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97 A. L. Benabid . S. Chabardes . E. Seigneuret

10 History of Stereotactic and Functional Neurosurgery in Canada . . . . . . . . . . . . . . . 113 A. G. Parrent

xiv

Table of contents

11 History of Stereotactic Surgery in China . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125 F.-C. Lee . B. Sun . J. Zhang . K. Zhang . F.-G. Meng

12 History of Stereotactic Surgery in India . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155 P. K. Doshi

13 History of Stereotactic Surgery in Korea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171 S. S. Chung

14 History of Stereotactic Surgery in Spain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 179 J. Guridi . M. Manrique

15 History of Stereotactic Neurosurgery in Italy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193 A. Franzini . V. A. Sironi . G. Broggi

16 History of Stereotactic and Functional Neurosurgery in Brazil . . . . . . . . . . . . . . . . 197 O. Vilela Filho

Section 2 Imaging in Stereotactic Surgery . . . . . . . . . . . . . . . . . . . . . . . 249 17 General Imaging Modalities: Basic Principles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 251 A. A. Gorgulho . W. Ishida . A. A. F. De Salles

18 CT/MRI Technology: Basic Principles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 269 M. I. Hariz . L. Zrinzo

19 CT/MRI Safety in Functional Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 279 M. Schulder . A. Oubre´

20 Functional MRI in Image Guided Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . 287 T. Sankar . G. R. Cosgrove

21 Angiography, MRA in Image Guided Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . 299 P. Jabbour . S. Tjoumakaris . R. Rosenwasser

22 Diagnostic PET in Image Guided Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . 307 B. Ballanger . T. van Eimeren . A. P. Strafella

23 Neurophysiologic Mapping for Glioma Surgery: Preservation of Functional Areas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 325 R. M. Richardson . M. S. Berger

Table of contents

24 Image Reconstruction and Fusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 335 B. A. Kall

Section 3 Stereotactic Targeting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 345 25 Printed Stereotactic Atlases, Review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 347 R. J. Coffey

26 Electronic Stereotactic Atlases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 373 J. Yelnik . E. Bardinet . D. Dormont

27 Anatomical and Probabilistic Functional Atlases in Stereotactic and Functional Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 395 W. L. Nowinski

28 Accuracy in Stereotactic and Image Guidance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 443 A. Hartov . D. W. Roberts

29 Development of a Classic: The Todd-Wells Apparatus, the BRW, and the CRW Stereotactic Frames . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 453 J. Arle

30 Leksell Stereotactic Apparatus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 469 L. D. Lunsford . D. Kondziolka . D. Leksell

31 The Riechert/Mundinger Stereotactic Apparatus . . . . . . . . . . . . . . . . . . . . . . . . . . . 487 J. K. Krauss

32 The Talairach Stereotactic System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 495 A. L. Benabid . S. Chabardes . E. Seigneuret . D. Hoffmann . J. F. LeBas

33 Laitinen Stereotactic Apparatus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 511 M. I. Hariz . L. V. Laitinen

34 Miniframe Stereotactic Apparatus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 521 M. A. Madera . W. D. Tobler

Section 4 Image Guided Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . 533 35 Engineering Aspects of Electromagnetic Localization in Image Guided Surgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 535 E. C. Parker . P. J. Kelly

xv

xvi

Table of contents

36 The History, Current Status, and Future of the StealthStation Treatment Guidance System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 543 R. Bucholz . L. McDurmont

37 BrainLab Image Guided System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 567 J. F. Fraser . T. H. Schwartz . M. G. Kaplitt

38 Robotic Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 583 P. L. Gildenberg

39 MRI in Image Guided Surgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 599 M. Schulder . L. Jarchin

40 CT in Image Guided Surgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 619 D. Kondziolka . L. D. Lunsford

41 Impedance Recording in Central Nervous System Surgery . . . . . . . . . . . . . . . . . . . 631 R. J. Andrews . J. Li . S. A. Kuhn . J. Walter . R. Reichart

42 Stereotactic and Image-Guided Biopsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 645 J. B. Elder . A. P. Amar . M. L. J. Apuzzo

43 Pathology Techniques in Stereotactic and Image Guided Biopsy . . . . . . . . . . . . . . 663 P. T. Chandrasoma . N. E. Klipfel

44 Stereotactic and Image Guided Craniotomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 679 E. C. Parker . P. J. Kelly

45 Image Guided Craniotomy for Brain Tumor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 699 I. E. McCutcheon

46 Virtual Reality in the Operating Room . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 725 P. L. Gildenberg

47 Comprehensive Brain Tumor Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 735 M. Tamber . M. Bernstein

48 Novel Therapies for Brain Tumors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 749 G. Al-Shamy . R. Sawaya

49 Image-Guided Management of Brain Abscess . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 769 E. Taub . A. M. Lozano

Table of contents

50 Image-Guided Management of Brain Stem Lesions . . . . . . . . . . . . . . . . . . . . . . . . . 779 M. Levivier

51 Stereotactic Approaches to the Brain Stem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 789 L. U. Zrinzo . D. G. T. Thomas

52 Image Guided Management of Intracerebral Hematoma . . . . . . . . . . . . . . . . . . . . . 797 A. Losiniecki . G. Mandybur

53 Technical Aspects of Image-Guided Neuroendoscopy . . . . . . . . . . . . . . . . . . . . . . . 807 J. D. Caird . J. M. Drake

54 Intraoperative Image Guidance in Skull Base Tumors . . . . . . . . . . . . . . . . . . . . . . . 815 D. Omahen . F. Doglietto . D. Mukherjee . F. Gentili

55 Image Guided Management of Cerebral Metastases . . . . . . . . . . . . . . . . . . . . . . . . 831 P. Kongkham . M. Bernstein

Section 5 Stereotactic Radiosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . 851 56 Radiobiology of Stereotactic Radiosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 853 D. C. Shrieve . J. S. Loeffler

57 Overview of Radiosurgery Technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 867 M. Schulder

58 Gamma Knife: Technical Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 897 D. J. Schlesinger . C. P. Yen . C. Lindquist . L. Steiner

59 Linac Radiosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 929 W. A. Friedman . F. J. Bova

60 CyberKnife: Technical Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 949 J. R. Adler . D. W. Schaal . A. Muacevic

61 Proton Beam Radiotherapy: Technical and Clinical Aspects . . . . . . . . . . . . . . . . . . 957 S. Y. Woo

62 IMRT: Technical and Clinical Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 965 M. P. Carol

63 What Every Neurosurgeon Should Know About Stereotactic Radiosurgery . . . . . . 977 P. M. Black . F. Tariq

xvii

xviii

Table of contents

64 Radiosensitizers in Neurooncology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 987 D. Khuntia . A. Chakravarti . H. I. Robins . K. Palanichamy . M. P. Mehta

65 Gamma Knife: Clinical Experience . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1007 A. Niranjan . L. D. Lunsford . J. C. Flickinger . J. Novotny . J. Bhatnagar . D. Kondziolka

66 Gamma Knife: Clinical Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1037 L. Steiner . C. P. Yen . J. Jagannathan . D. Schlesinger . M. Steiner

67 Linac Radiosurgery: Technical Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1087 F. J. Bova . W. A. Friedman

68 Cyberknife: Clinical Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1111 F. C. Henderson Sr . W. Jean . N. Nasr . G. Gagnon

69 Proton Beam Radiosurgery: Clinical Experience . . . . . . . . . . . . . . . . . . . . . . . . . . . 1131 H. A. Shih . P. H. Chapman . J. S. Loeffler

70 Radiosurgery for Metastases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1139 M. Maarouf . C. Bu¨hrle . M. Kocher . V. Sturm

71 Focused and Conventional Radiation for Acoustic Nerve Tumors . . . . . . . . . . . . . 1151 R. Den . S. H. Paek . D. W. Andrews

72 Radiosurgery for Pituitary Tumors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1171 J. P. Sheehan . J. Jagannathan . W. J. Elias . E. R. Laws

73 Radiosurgery for Functional Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1191 D. Kondziolka

74 Whole Body and Spinal Radiosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1203 P. C. Gerszten

75 Gamma Knife Radiosurgery: Technical Issues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1225 D. Kondziolka . A. Niranjan . J. Novotny . J. Bhatanagar . L. D. Lunsford

Section 6 Functional Neurosurgery – Technical Aspects . . . . . . . . . 1237 76 Image Guided Functional Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1239 S. Khan . N. K. Patel . E. White . P. Plaha . S. Ashton . S. S. Gill

77 Evoked Potentials in Functional Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1255 J. L. Shils . J. E. Arle

Table of contents

78 Microelectrode Recording in Functional Neurosurgery . . . . . . . . . . . . . . . . . . . . . 1283 W. D. Hutchison . J. O. Dostrovsky . M. Hodaie . K. D. Davis . A. M. Lozano . R. R. Tasker

79 Impedance Recording in Functional Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . 1325 L. Zrinzo . M. I. Hariz

80 Anesthesia for Functional Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1331 P. H. Manninen . N. Apichatibutra

81 Lesions Versus Implanted Stimulators in Functional Neurosurgery . . . . . . . . . . . 1349 W. S. Anderson . R. E. Clatterbuck . K. Kobayashi . J.-H. Kim . F. A. Lenz

82 Radiofrequency Lesions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1359 E. R. Cosman Sr. . E. R. Cosman Jr.

83 Stimulation Physiology in Functional Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . 1383 A. W. Laxton . J. O. Dostrovsky . A. M. Lozano

84 Stimulation Technology in Functional Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . 1401 B. H. Kopell . A. Machado . C. Butson

85 Therapeutic Lesions Through Chronically Implanted Deep Brain Stimulation Electrodes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1427 S. Raoul . D. Leduc . C. Deligny . Y. Lajat

Section 7 Functional Neurosurgery for Movement and Motor Disorders – Clinical Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . 1443 86 Surgery for Movement Disorders: An Overview . . . . . . . . . . . . . . . . . . . . . . . . . . . 1445 K. M. Prakash . A. E. Lang

87 History of Surgery for Movement Disorders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1467 A. G. Parrent

88 Psychiatric Considerations in Management of Movement Disorders . . . . . . . . . . 1487 M. Zurowski . V. Voon . V. Valerie

89 Pathophysiology of Parkinson’s Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1497 M. R. DeLong . T. Wichmann

90 Medical Management of Parkinson’s Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1507 E. V. Encarnacion . R. A. Hauser

xix

xx

Table of contents

91 Patient Selection for Surgery for Parkinson’s Disease . . . . . . . . . . . . . . . . . . . . . . 1529 E. K. Tan . J. Jankovic

92 Pallidotomy for Parkinson’s Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1539 M. I. Hariz

93 Selective Thalamotomy and Gamma Thalamotomy for Parkinson Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1549 C. Ohye

94 Subthalamotomy for Parkinson’s Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1569 J. A. Obeso . L. Alvarez . R. Macias . N. Pavon . G. Lopez . R. Rodriguez-Rojas . M. C. Rodriguez-Oroz . J. Guridi

95 Globus Pallidus Stimulation for Parkinson’s Disease . . . . . . . . . . . . . . . . . . . . . . . 1577 M. Deogaonkar . J. L. Vitek

96 Subthalamic Nucleus Stimulation for Parkinson’s Disease . . . . . . . . . . . . . . . . . . . 1603 A. L. Benabid . J. Mitrofanis . S. Chabardes . E. Seigneuret . N. Torres . B. Piallat . A. Benazzouz . V. Fraix . P. Krack . P. Pollak . S. Grand . J. F. LeBas

97 Thalamic Stimulation for Parkinson’s Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1631 R. E. Wharen . R. J. Uitti . J. A. Lucas

98 PPN Stimulation for Parkinson’s Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1649 S. Stone . C. Hamani . A. M. Lozano

99 Other Targets to Treat Parkinson’s Disease (Posterior Subthalamic Targets and Motor Cortex) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1665 F. Velasco . S. Palfi . F. Jime´nez . J. D. Carrillo-Ruiz . G. Castro . Y. Keravel

100 Motor Cortex Stimulation for Parkinson’s Disease . . . . . . . . . . . . . . . . . . . . . . . . . 1679 M. Meglio . B. Cioni

101 Tissue Transplantation for Parkinson’s Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . 1691 K. Mukhida . M. Hong . I. Mendez

102 Gene Transfer for Parkinson’s Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1719 P. A. Starr . K. S. Bankiewicz

103 Intraparenchymal Drug Delivery for Parkinson’s Disease . . . . . . . . . . . . . . . . . . . 1731 R. D. Penn . A. A. Linninger

Table of contents

104 Management of Essential Tremor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1743 J. M. Nazzaro . K. E. Lyons . R. Pahwa

105 Management of Tremors other than Essential Tremor and Parkinson’s Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1757 J. P. Nguyen . S. Raoul . C. Deligny . V. Roualdes . Y. Keravel

106 Diagnosis and Medical Management of Dystonia . . . . . . . . . . . . . . . . . . . . . . . . . . 1767 S. Fahn

107 Pathophysiology of Dystonia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1779 J. A. Bajwa . M. D. Johnson . J. L. Vitek

108 Central Procedures for Primary Dystonia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1801 X. A. Vasques . L. Cif . B. Biolsi . P. Coubes

109 Functional Stereotactic Procedures for Treatment of Secondary Dystonia . . . . . 1835 H-H. Capelle . J. K. Krauss

110 Diagnosis and Medical Management of Cervical Dystonia . . . . . . . . . . . . . . . . . . . 1857 R. Bhidayasiri . D. Tarsy

111 Central Procedures for Cervical Dystonia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1871 J. Q. Oropilla . Z. H. T. Kiss

112 Peripheral Procedures for Cervical Dystonia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1885 T. Taira

113 Microvascular Decompression for Trigeminal Neuralgia . . . . . . . . . . . . . . . . . . . . 1911 J. R. Pagura

114 History and Current Neurosurgical Management of Spasticity . . . . . . . . . . . . . . . 1925 R. D. Penn

115 Destructive Neurosurgical Procedures for Spasticity . . . . . . . . . . . . . . . . . . . . . . . 1935 M. Sindou . P. Mertens

116 Surgery in the Dorsal Root Entry Zone for Spasticity . . . . . . . . . . . . . . . . . . . . . . . 1959 M. P Sindou . P. Mertens

117 Intrathecal Drugs for Spasticity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1973 R. D. Penn

xxi

xxii

Table of contents

Section 8 Functional Neurosurgery for Pain . . . . . . . . . . . . . . . . . . . . 1983 118 Anatomy and Physiology of Cancer Pain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1985 W. D. Willis Jr. . K. N. Westlund

119 Neuroimaging and Pain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2019 R. Peyron

120 What have PET Studies Taught us about Cerebral Mechanisms Involved in Analgesic Effect of DBS? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2031 R. Kupers . J. Gybels

121 History of DBS for Pain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2049 D. Richardson

122 Comprehensive Management of Cancer Pain Including Surgery . . . . . . . . . . . . . . 2061 P. S. Kalanithi . J. M. Henderson

123 The Central Lateral Thalamotomy for Neuropathic Pain . . . . . . . . . . . . . . . . . . . . 2081 D. Jeanmonod . A. Morel

124 Technique of Trigeminal Nucleotractotomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2097 M. J. Teixeira . E. T. Fonoff

125 Bulbar DREZ Procedures for Facial Pain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2125 J. P. Gorecki

126 Percutaneous Cordotomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2137 R. R. Tasker

127 CT-Guided Percutaneous Cervical Cordotomy for Cancer Pain . . . . . . . . . . . . . . . 2149 Y. Kanpolat

128 Ablative Spinal Cord Procedures for Cancer Pain . . . . . . . . . . . . . . . . . . . . . . . . . . 2159 P. L. Gildenberg

129 Intrathecal Opiates for Cancer Pain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2171 J. C. Sol . J. C. Verdie . Y. Lazorthes

130 Management of Pain of Benign Versus Cancer Origin . . . . . . . . . . . . . . . . . . . . . . 2197 P. L. Gildenberg . R. A. DeVaul

Table of contents

131 DBS for Persistent Non-Cancer Pain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2227 C. Hamani . D. Fontaine . A. Lozano

132 Motor Cortex Stimulation for Persistent Non-Cancer Pain . . . . . . . . . . . . . . . . . . . 2239 A. G. Machado . A. Y. Mogilner . A. R. Rezai

133 Radiofrequency Dorsal Root Entry Zone Lesions for Pain . . . . . . . . . . . . . . . . . . . 2251 P. Konrad . F. Caputi . A. O. El-Naggar

134 Surgical Dorsal Root Entry Zone Lesions for Pain . . . . . . . . . . . . . . . . . . . . . . . . . . 2269 M. P. Sindou

135 Facet Denervation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2291 R. R. Tasker . Wen Ching Tzaan

136 Sympathectomy for Pain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2297 C. R. Telles-Ribeiro . L. F. de Oliveira

137 Spinal Cord Stimulation. Techniques, Indications and Outcome . . . . . . . . . . . . . . 2305 B. Linderoth . B. A. Meyerson

138 Mechanisms of Action of Spinal Cord Stimulation . . . . . . . . . . . . . . . . . . . . . . . . . 2331 B. Linderoth . R. D. Foreman . B. A. Meyerson

139 Peripheral Nerve Stimulation for Neuropathic Pain . . . . . . . . . . . . . . . . . . . . . . . . 2349 A. G. Shetter

140 The Pathophysiology of Trigeminal Neuralgia . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2359 R. W. Hurt

141 Radiofrequency Rhizotomy for Trigeminal Neuralgia . . . . . . . . . . . . . . . . . . . . . . . 2421 E. Taub

142 Retrogasserian Glycerol Injection for Trigeminal Neuralgia . . . . . . . . . . . . . . . . . 2429 B. Linderoth . G. Lind

143 Balloon Compression for Trigeminal Neuralgia . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2457 J. A. Brown . J. G. Pilitsis

144 Microvascular Decompression for Trigeminal Neuralgia . . . . . . . . . . . . . . . . . . . . 2465 S. Sup Chung

145 Gamma Knife Surgery for Trigeminal Neuralgia and Facial Pain . . . . . . . . . . . . . . 2475 A. C. J. de Lotbinie`re

xxiii

xxiv

Table of contents

146 Treatment of Headache . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2483 N. T. Mathew

147 Occipital Neuralgia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2507 D. B. Cohen . M. Y. Oh . D. M. Whiting

148 Hypothalamic Stimulation for Cluster Headache . . . . . . . . . . . . . . . . . . . . . . . . . . 2517 A. Franzini . M. Leone . G. Messina . R. Cordella . C. Marras . G. Bussone . G. Broggi

149 Surgical Treatment of Chronic Cluster Headache . . . . . . . . . . . . . . . . . . . . . . . . . . 2525 J. M. Castilla

150 Mesencephalotomy for Cancer Pain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2533 P. L. Gildenberg

Section 9 Management of Epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2541 151 Indications for Surgical Management of Epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . 2543 H. G. Wieser . D. Zumsteg

152 Classification of Epileptic Seizures and Epilepsies . . . . . . . . . . . . . . . . . . . . . . . . . 2561 H. O. Lu¨ders . S. Noachtar

153 EEG in Epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2575 M. Hoppe . R. Wennberg . P. Tai . B. Pohlmann-Eden

154 The Wada Test-60th Year Anniversary Update-In Epilepsy Surgery . . . . . . . . . . . 2587 J. A. Wada . B. Kosaka

155 Imaging Evaluation of Epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2617 D. Madhavan . R. Kuzniecky

156 Image Guided Epilepsy Surgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2633 Y. G. Comair . R. B. Chamoun

157 Intraoperative Monitoring in Epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2651 G. Ojemann

158 MEG in Epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2661 A. Fujimoto . T. Akiyama . H. Otsubo

159 Medical Management of Epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2669 M. E. Newmark

Table of contents

160 Selective Amygdalo-Hypocampectomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2677 T. A. Valiante

161 Subpial Transection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2715 Z. S. Tovar-Spinoza . J. T. Rutka

162 Corpus Callosotomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2723 R. E. Maxwell

163 Hemispherectomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2741 J.- G. Villemure . R. T. Daniel

164 Radiosurgery in Epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2761 I. Yang . N. M. Barbaro

165 Centromedian Thalamic Stimulation for Epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . 2777 F. Velasco . A. L. Velasco . M. Velasco . F. Jime´nez . J. D. Carrillo-Ruiz . G. Castro

166 Anterior Nucleus DBS in Epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2793 M. Hodaie . C. Hamani . R. Wennberg . W. Hutchison . J. Dostrovky . A. M. Lozano

167 Vagal Nerve Stimulation for Seizures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2801 A. P. Amar . J. B. Elder . M. L. J. Apuzzo

168 Cerebellar Stimulation for Seizure Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2823 R. Davis

169 Stimulation of the Hippocampus and the Seizure Focus . . . . . . . . . . . . . . . . . . . . 2839 A. L. Velasco . F. Velasco . M. Velasco . G. Castro . J. D. Carrillo-Ruiz . J. M. Nu´n˜ez D. Trejo

Section 10 Psychiatric Surgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2853 170 Ethical Considerations in Psychiatric Surgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2855 B. S. Appleby . P. V. Rabins

171 Psychosurgery – A Historical Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2867 C. R. Bjarkam . J. C. Sørensen

172 Cingulotomy for Depression and OCD . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2887 G. R. Cosgrove

xxv

xxvi

Table of contents

173 DBS for OCD . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2897 L. Gabrie¨ls . P. Cosyns . K. van Kuyck . B. Nuttin

174 Medical Management and Indications for Surgery in Depression . . . . . . . . . . . . . 2925 P. Giacobbe . S. Kennedy

175 Ablative Procedures for Depression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2943 V. A. Coenen . C. R. Honey

176 Deep Brain Stimulation for Depression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2953 C. Hamani . B. Snyder . A. Laxton . A. Lozano

177 Surgical Procedures for Tourette’s Syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2963 V. Visser-Vandewalle

178 Treatment of Aggressive Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2971 G. Broggi . A. Franzini

Section 11 Special and Emerging Applications . . . . . . . . . . . . . . . . . . 2979 179 DBS Disorders of Consciousness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2981 N. D. Schiff

180 Apnea: Phrenic Nerve Stimulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2991 S. Rehncrona . G. Sedin . H. Fodstad

181 DBS for Bladder Dysfunction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2999 R. Almusa . M. M. Hassouna

182 Impaired Vision: Visual Prosthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3009 J. P. Girvin . A. G. Martins

183 Impaired Hearing: Auditory Prosthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3021 J. K. Niparko . A. Marlowe . H. W. Francis

184 Impaired Motor Function: Functional Electrical Stimulation . . . . . . . . . . . . . . . . . 3047 R. B. Stein . A. Prochazka

185 Gene Therapy for Neurological Disorders (Except Oncology) . . . . . . . . . . . . . . . . 3061 M. G. Kaplitt

Table of contents

186 Gene Therapy for Brain Tumors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3083 M. L. M. Lamfers . E. A. Chiocca

187 Microdialysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3117 M. J. Smith . M. G. Kaplitt

Section 12 The Future of Stereotactic and Functional Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3129 188 The Future of Computers and Imaging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3131 B. A. Kall

189 The Future of Neuronavigation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3137 D. W. Roberts

190 The Future of Radiosurgery and Radiotherapy . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3143 L. Ma . P. K. Sneed

191 The Future of Infusion Systems in Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . 3155 R. D. Penn

192 The Future of Cell Transplantation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3161 M. B. Newman . R. A. E. Bakay

193 The Future of Neural Interface Technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3185 M. C. Park . M. A. Goldman . T. W. Belknap . G. M. Friehs

194 The Future of Molecular Neuro-Oncology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3201 J. A. J. King . M. D. Taylor

195 Future Ethical Challenges in Neurosurgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3229 N. Lipsman . M. Bernstein

Subject Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3239

xxvii

List of Contributors

John R. Adler, Jr. Department of Neurosurgery, Stanford University, Stanford, CA, USA

Women’s Hospital, 75 Francis Street, CA 138F, Boston, MA 02115, USA Email: [email protected]

Tomoyuki Akiyama Division of Neurology, Department of Pediatrics, The Hospital for Sick Children, University of Toronto, 555 University Avenue, Toronto, Ontario, M5G 1X8, Canada

David W. Andrews Department of Neurosurgery, Jefferson Medical College, 834 Walnut St. Suite 650, PA 19107, Philadelphia, USA Email: [email protected]

Riyad Almusa Toronto Western Hospital, 399 Bathurst St, M5T 2S8, Toronto, Ontario, Canada George Al-Shamy Department of Neurosurgery - 442, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Blvd., Houston, TX 77030, USA L. Alvarez Movement Disorders, Functional Neurosurgery and Neurophysiology Units, Centro Internacional de Restauracion Neurologica (CIREN), Havana, Cuba Arun Paul Amar Departments of Neurosurgery, University of California San Francisco and the Permanente Medical Group 2025 Morse Avenue, Sacramento, CA 95825, USA Email: [email protected] William S. Anderson Instructor in Neurosurgery, Harvard Medical School, Department of Neurological Surgery, Brigham and

Russell J. Andrews Ames Associate (Smart Systems and Nanotechnology), NASA Ames Research Center, CA 94035, Moffett Field, USA Email: [email protected] Narisa Apichatibutra Department of Anesthesia, Toronto Western Hospital, University Health Network, University of Toronto, Toronto, Ontario, Canada Brian S. Appleby John Hopkins Hospital, Meyer 279, 600 N. Wolfe St., 21287–7279, MD, Baltimore, USA Michael L. J. Apuzzo Edwin M. Todd/Trent H. Wells, Jr., Professor of Neurological Surgery and Professor of Radiation Oncology, Biology, and Physics Keck School of Medicine, University of Southern California, 1200 North State Street, Suite 5046, Los Angeles, CA 90033, USA Email: [email protected]

xxx

List of contributors

Jeffrey E. Arle Department of Neurosurgery, Lahey Clinic, 41 Mall Road, 01805, Burlington, MA, USA

Eric Bardinet INSERM U679, Hoˆpital de la Salpeˆtrie`re, 47, Bd de l’Hoˆpital, 75013, Paris, France

Sharon Ashton Renishaw plc, New Mills, Wotton-under-Edge, Gloucestershire GL12 8JR, UK

Thomas Belknap Department of Clinical Neurosciences, Program in Neurosurgery, The Warren Alpert Medical School of Brown University, Rhode Island Hospital, Providence, RI 02903, USA

Tipu Z. Aziz Oxford Functional Neurosurgery, Nuffield Department of Surgery, University of Oxford, and Department of Neurological Surgery, The West Wing, The John Radcliffe Hospital, Oxford. Imperial College London and Charing Cross Hospital, London Jawad A. Bajwa Capistrant Parkinson and Movement Disorder Center, Bethesda Hospital and Nasseff Neuroscience Center, United Hospital, Saint Paul, MN, USA Neurological Associates of Saint Paul, Maplewood, MN, USA Roy A. E. Bakay Department of Neurosurgery, Rush University Medical Center, Chicago IL, USA Email: [email protected] B. Ballanger PET Imaging Centre, Center of Addiction Mental Health, University of Toronto, Toronto, Ontario, Canada Krystof S. Bankiewicz Department of Neurological Surgery, University of California, San Francisco, USA Nicholas M. Barbaro Department of Neurological Surgery, University of California, San Francisco, USA

Alim-Louis Benabid Joseph Fourier University, Pavillon B - Grenoble University Hospital, Grenoble, France Email: [email protected] Abdelhamid Benazzouz University of Bordeaux, France Mitchel S. Berger Department of Neurological Surgery, University of California, 505 Panassus Ave, Box 0112, San Francisco, CA, USA Email: [email protected] Mark Bernstein Division of Neurosurgery, Toronto Western Hospital and University of Toronto, Toronto, Canada Email: [email protected] Jagdish Bhatnagar The Center for Image-Guided Neurosurgery, University of Pittsburgh Medical Center, Pittsburgh, PA 15213, USA Roongroj Bhidayasiri Chulalongkorn Comprehensive Movement Disorders Center, Chulalongkorn University Hospital, 1873 Rama 4 Road, Bangkok 10330, Thailand Email: [email protected]

List of contributors

B. Biolsi CHRU Montpellier, Service de Neurochirurgie, Universite´ Montpellier I, Montpellier, France

Chris Butson Medical School of Wisconsin, 8701 Watertown Plank Road, WI 53226, Milwaukee, USA

Carsten Reidies Bjarkam Department of Neurobiology, Institute of Anatomy, University of Aarhus, DK–8000 Aarhus C, Denmark Email: [email protected]

John D. Caird Division of Neurosurgery, Department of Surgery, The Hospital for Sick Children, University of Toronto, 555 University Avenue, M5G 1X8, Toronto, Ontario, Canada

Peter M. Black Department of Neurosurgery, Brigham and Women’s Hospital, 75 Francis St, Boston, MA 02115, USA Email: [email protected] Frank J. Bova Department of Neurological Surgery, University of Florida, PO Box 100265, Gainesville, FL 32610, USA Giovanni Broggi Department of Neurosurgery, Fondazione Istituto Neurologico “C. Besta”, Milan, Italy Email: [email protected] Jeffrey A. Brown 600 Northern Boulevard #118, Great Neck, NY 11021, USA Email: [email protected] Richard Bucholz Division of Neurosurgery, Department of Surgery, Saint Louis University School of Medicine, Saint Louis, Missouri, USA Email: [email protected] Christian Bu¨hrle Associate Professor, Department of Stereotactic and Functional Neurosurgery, University Hospital, 50924 Cologne, Germany G. Bussone Department of Neurosurgery, Neurological Institute Foundation “C. Besta”, Milan, Italy

Hans-Holger Capelle Department of Neurosurgery, Medical School Hannover, MHH, Hannover, Germany Franco Caputi Department of Neurosurgery, Rome, Italy Email: [email protected] Mark P. Carol 744 Lexington Way, Burlingame, CA 94010, USA Email: [email protected] Jose´ Damia´n Carrillo Epilepsy Surgery Clinic; Unit for Stereotactic, Functional Neurosurgery and Radiosurgery, General Hospital of Mexico City, Mexico Jose´ Manuel Castilla Servicio de Neurocirugı´a, Hospital “General Yagu¨e”, Avenida de Cid 96, 09005, Burgos, Spain Email: [email protected] Guillermo Castro Epilepsy Surgery Clinic; Unit for Stereotactic, Functional Neurosurgery and Radiosurgery, General Hospital of Mexico City, Mexico Stephan Chabardes Joseph Fourier University, Pavillon B - Grenoble University Hospital, 38700, Grenoble, France Arnab Chakravarti Massachusetts General Hospital, Department of

xxxi

xxxii

List of contributors

Radiation Oncology, Cox 3, 100 Blossom Street, Boston, MA, USA Email: [email protected] Roukoz B. Chamoun Department of Neurosurgery, Baylor College of Medicine, Houston, Texas, USA Parakrama T. Chandrasoma Department of Pathology, Keck School of Medicine University of Southern California, GNH 2900, 1200 North State St., CA, USA Paul H. Chapman Departments of Radiation Oncology and Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA Email: [email protected] E. Antonio Chiocca James Cancer Hospital/Solove Research Institute, The Ohio State University Medical Center, Columbus, OH 43210–1240, USA Email: [email protected] Sang Sup Chung Bundang CHA General Hospital, 351 Yatap-dong, 463–712, Bundang-gu Sungnam-se, Kyong-doSungnam, South Korea Email: [email protected] L. Cif CHRU Montpellier, Service de Neurochirurgie, Universite´ Montpellier I, Montpellier, France Beatrice Cioni Neurochirurgia Funzionale e Spinale, Universita` Cattolica, Roma, Italy Richard E. Clatterbuck Hattiesburg Clinic, 4155 28th Avenue, Hattiesburg,

MS 39401, USA Email: [email protected] Volker A. Coenen Surgical Center for Movement Disorders, Division of Neurosurgery, University of British Columbia, Vancouver, BC, Canada Robert J. Coffey Medtronic Neurological, 4000 Lexington Avenue North, MN, USA Email: [email protected] David B. Cohen Drexel University College of Medicine Department of Neurosurgery, Allegheny General Hospital, 420 East North Ave, PA 15212, Pittsburgh, USA Youssef G. Comair Department of Neurosurgery, Baylor College of Medicine, 1709 Dryden, TX 77030, Houston, Texas, USA Email: [email protected] R. Cordella Department of Neurosurgery, Neurological Institute Foundation “C. Besta”, Milan, Italy G. Rees Cosgrove Department of Neurosurgery, Lahey Clinic Medical Center and Tufts University School of Medicine, Boston, Massachusetts, USA Email: [email protected] Eric R. Cosman, Jr. Cosman Medical, 76 Cambridge Street, MA, Burlington, USA Email: [email protected] Eric R. Cosman, Sr. Cosman Medical, 76 Cambridge Street, MA, Burlington, USA Email: [email protected]

List of contributors

Paul Cosyns Department of Psychiatry, University Hospital Antwerp, Antwerp, Belgium

Woodruff Memorial Research Building, 101 Woodruff Circle, Atlanta, GA 30322, USA Email: [email protected]

Philippe Coubes Unite´ de Recherche sur les Mouvements Anormaux, Hoˆpital Gui de Chauliac, Service de Neurochirurgie, 80 Avenue Augustin Fliche, 34295 Montpellier cedex 05, France Email: [email protected]

Robert Den Department of Neurosurgery, Jefferson Medical College, 834 Walnut St. Suite 650, PA 19107, Philadelphia, USA

Karen D. Davis Department of Physiology, University of Toronto, 1 King’s College Circle, M5S 1S8, Toronto, Canada

Milind Deogaonkar Functional Neuroscience Research Center, Cleveland Clinic Lerner Research Center, 9500 Euclid Avenue, OH 44195, Cleveland, USA

Ross Davis Neural Engineering Clinic, 330 Hammock Shore Dr., Melbourne Beach, FL, 32951, USA Email: [email protected]

Richard A. DeVaul Prof. Psychiatry, College of Medicine, Texas A & M System Health Science Center, College Station, Texas, USA

Alain C. J. de Lotbinie`re FACS Brain & Spine Surgeons of New York, 244 Westchester Avenue, NY 10604, White Plains, USA Email: [email protected]

John P. Donoghue Department of Neuroscience and Brain Science Program, Brown University, Providence, RI 02912, USA

Luiz F. de Oliveira Neurodor - Neurosurgery and Pain Clinic, Rua Visconde de Piraja 351/509, Cep: 22471–002, Ipanema, Rio de Janeiro, RJ, Brazil Antonio A. F. De Salles Department of Neurosurgery, David Geffen School of Medicine, University of California Los Angeles, 10495 Le Conte Avenue, Suite 2120, Los Angeles, California 90095, USA Email: [email protected] Ce´line Deligny Department of Neurology, CHU de Nantes, Nantes, France Mahlon R. DeLong Department of Neurology, Emory University

Paresh K. Doshi Department of Neuroscience, Jaslok Hospital and Research Centre, 15 - Dr. Deshmukh Marg, Pedder Road, Mumbai 400 026, Maharashtra, India Email: [email protected] Jonathan O. Dostrovsky Department of Physiology, University of Toronto, 1 King’s College Circle, M5S 1S8, Toronto, Canada Email: [email protected] James M. Drake Division of Neurosurgery, Department of Surgery, The Hospital for Sick Children, University of Toronto, 555 University Avenue, M5G 1X8, Toronto, Ontario, Canada Email: [email protected]

xxxiii

xxxiv

List of contributors

James B. Elder Department of Neurological Surgery, Keck School of Medicine, University of Southern California, 1200 North State Street, Suite 5046, Los Angeles, CA 90033, USA Email: [email protected]

Sa˜o Paulo Medical School, Rua Mena Barreto 765 - Itaim Bibi, SP- 014033–010, Sa˜o Paulo, Brazil

Jeff Elias Department of Neurosurgery, University of Virginia, Box 800212, HSC, VA, 22908–0212, Charlottesville, USA Email: [email protected]

Robert D. Foreman Department of Physiology, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA

Amr O. El-Naggar Lake Cumberland Neurosurgery, Somerset, KY, USA Email: [email protected] Elmyra V. Encarnacion Plummmer Movement Disorders Center, Texas A & M Health Sciences Center/Scott & White, Temple, Texas, USA Stanley Fahn Department of Neurology, Columbia University College of Physicians & Surgeons, New York, NY 10032, USA Email: [email protected] Osvaldo Vilela Filho Goiaˆnia Neurological Institute, Goiaˆnia, GO, Brazil Email: [email protected] John C. Flickinger The Departments of Neurological Surgery, and Radiation Oncology The Center for Image-Guided Neurosurgery, University of Pittsburgh Medical Center, Pittsburgh, PA 15213, USA Harald Fodstad University of Uppsala, Uppsala, Sweden Erich Talamoni Fonoff Division of Functional Neurosurgery, University of

Denys Fontaine Service de Neurochirurgie, Hoˆpital Pasteur, Centre Hospitalier Universitaire de Nice, Nice, France

Valerie Fraix Joseph Fourier University, Pavillon B - Grenoble University Hospital, 38700, Grenoble, France Doglietto Francesco Department of Neurosurgery, Toronto Western Hospital, 399 Bathurst Street, M5T 2S8, Toronto, Canada Howard W. Francis Department of Otolaryngology, Head & Neck Surgery, The Johns Hopkins School of Medicine, Baltimore, USA Angelo Franzini Department of Neurosurgery, Fondazione Istituto Neurologico “C. Besta”, Milan, Italy Justin F. Fraser Department of Neurological Surgery, Weill Medical College of Cornell University, New YorkPresbyterian Hospital, New York, NY, USA William A. Friedman Department of Neurological Surgery, University of Florida, PO Box 100265, Gainesville, FL 32610, USA Email: [email protected] Gerhard M. Friehs Department of Clinical Neurosciences, Program in Neurosurgery, The Warren Alpert Medical School of Brown University, Rhode Island Hospital, Providence, RI 02903, USA

List of contributors

Ayataka Fujimoto Division of Neurology, Department of Pediatrics, The Hospital for Sick Children, University of Toronto, 555 University Avenue, Toronto, Ontario, M5G 1X8, Canada

John P. Girvin 1078 The Parkway, ON, N6A 2W0, London, Canada Email: [email protected]

Loes Gabrie¨ls Department of Psychiatry, University Hospital Gasthuisberg, Leuven, Belgium

Marc A. Goldman Department of Clinical Neurosciences, Program in Neurosurgery, The Warren Alpert Medical School of Brown University, Rhode Island Hospital, Providence, RI 02903, USA

Gregory Gagnon Department of Neurosurgery and Radiation Medicine, Georgetown University Hospital, 3800 Reservoir Rd, 20007, Washington DC, USA

John P. Gorecki Department of Neurosurgery, Wichita Surgical Specialists, P.A. The Heritage Plaza, 818 N. Emporia, Suite 200, 67214–3788, Wichita, Kansas, USA Email: [email protected]

Fred Gentili Department of Neurosurgery, Toronto Western Hospital, 399 Bathurst Street, M5T 2S8, Toronto, Canada Email: [email protected] Peter C. Gerszten Department of Neurological Surgery, University of Pittsburgh, UPMC Presbyterian B–400, 200 Lothrop Street, PA 15213, Pittsburgh, USA Email: [email protected]

Alessandra A. Gorgulho Department of Neurosurgery, David Geffen School of Medicine, University of California Los Angeles, 10495 Le Conte Avenue, Suite 2120, Los Angeles, California 90095, USA Sylvie Grand Joseph Fourier University, Pavillon B - Grenoble University Hospital, 38700, Grenoble, France

Peter Giacobbe University Health Network, University of Toronto, 200 Elizabeth Street, M5G 2C4, Toronto, Ontario, Canada

Alexander L. Green Oxford Functional Neurosurgery, Nuffield Department of Surgery, University of Oxford and Department of Neurological Surgery, The West Wing, The John Radcliffe Hospital, Oxford, UK

Philip L. Gildenberg Houston Stereotactic Concepts, 3776 Darcus St., 77005, Houston, Texas, USA Email: [email protected]

Jorge Guridi Division of Neurosurgery, Clinica Universitaria, Universidad de Navarra, Centro de Investigacio´n Medica Aplicada. CIMA, Pamplona, Spain

Steven S. Gill Department of Neurosurgery, Frenchay Hospital, Bristol BS16 1LE, UK Email: [email protected]

Jan Gybels Department of Neurosurgery, Gasthuisberg University Hospital, University of Leuven, Leuven, Belgium

xxxv

xxxvi

List of contributors

Sun Ha Paek Department of Neurosurgery, Jefferson Medical College, 834 Walnut St. Suite 650, PA 19107, Philadelphia, USA Clement Hamani Division of Neurosurgery, Department of Surgery, Toronto Western Hospital, University of Toronto, Toronto, Ontario, Canada Marwan I. Hariz Edmond J. Safra Chair of Functional Neurosurgery, Unit of Functional Neurosurgery, Institute of Neurology, London, UK Email: [email protected] Alex Hartov Thayer School of Engineering, Dartmouth College, Hannover, NH 03755, USA Magdy M. Hassouna Toronto Western Hospital, 399 Bathurst St, M5T 2S8, Toronto, Ontario, Canada Email: [email protected] Robert A. Hauser Parkinson’s Disease and Movement Disorders Center, University of South Florida, 4 Columbia Drive, Suite 410, Tampa, Florida 33606, USA Email: [email protected] Jaimie M. Henderson Stanford University Medical Center, 300 Pasteur Dr, CA 94305, Stanford, USA Email: [email protected] Fraser Cummins Henderson, Sr. Georgetown University Medical Center, 3800 Reservoir Rd, 20007, Washington DC, USA Email: [email protected] Leigh R. Hochberg Department of Neuroscience and Brain Science

Program, Brown University, Providence, RI 02912, USA Department of Neurology, Massachusetts General Hospital, Brigham and Women’s Hospital, Spaulding Rehabilitation Hospital, Harvard Medical School, Boston, MA, USA Center for Restorative and Regenerative Medicine, Rehabilitation Research and Development Service, Department of Veterans Affairs, Veterans Health Administration, Providence, RI 02908, USA Mojgan Hodaie Department of Physiology, University of Toronto, 1 King’s College Circle, M5S 1S8, Toronto, Canada Dominique Hoffmann Joseph Fourier University, Pavillon B - Grenoble University Hospital, Grenoble, France Christopher R. Honey Surgical Center for Movement Disorders - Division of Neurosurgery – University of British Columbia Vancouver, BC, Canada Email: [email protected] Murray Hong Departments of Anatomy & Neurobiology and Surgery (Neurosurgery), Dalhousie University, Halifax, Nova Scotia, Canada Matthias Hoppe Bethel Epilepsy Centre, Bielefeld, Germany R. Wayne Hurt Chief of Neurological Surgery, St. Joseph Medical Center and Assistant Clinical Professor of Neurological Surgery, Baylor College of Medicine and University of Texas Medical Branch, Houston, Texas, USA William Hutchison Department of Neurosurgery, Toronto Western Hospital, 399 Bathurst Street, M5S 2T8, Toronto, Ontario, Canada

List of contributors

Warren Ishida Department of Neurosurgery, David Geffen School of Medicine, University of California Los Angeles, 10495 Le Conte Avenue, Suite 2120, Los Angeles, California 90095, USA Pascal Jabbour Department of Neurosurgery, Philadelphia, PA, USA E-mail: [email protected] Jay Jagannathan Lars Leksell Center for Gamma Surgery, Department of Neurosurgery, University of Virginia, Charlottesville, VA, USA Joseph Jankovic Parkinson’s Disease Center and Movement Disorders Clinic, Department of Neurology, Baylor College of Medicine, 6550 Fannin, Suite 1801, Houston, Texas 77030, USA Email: [email protected]

Matthew D. Johnson Department of Biomedical Engineering, Cleveland Clinic Foundation, Cleveland, Ohio, USA Paul Kalanithi Stanford University Medical Center, 300 Pasteur Dr, CA 94305, Stanford, USA Bruce A. Kall Departments of Neurologic Surgery and Information Technology, Mayo Clinic, Rochester, MN, USA Email: [email protected] Yu¨cel Kanpolat Inkilap Sokak No: 24/2, 06640, Kizilay, Turkey Email: [email protected] Michael G. Kaplitt Department of Neurological Surgery, Weill Cornell Medical College, New York, NY, USA Email: [email protected]

Lauren Jarchin Department of Neurosurgery, North Shore LIJ, Manhasset, NY 11030, USA

Patrick J. Kelly Department of Neurological Surgery, NYU School of Medicine, 530 First Ave, Suite 8R, NY, USA Email: [email protected]

Walter Jean Department of Neurosurgery and Radiation Medicine, Georgetown University Hospital, 3800 Reservoir Rd, 20007, Washington DC, USA Email: [email protected]

Sidney Kennedy University Health Network, University of Toronto, 200 Elizabeth Street, M5G 2C4, Toronto, Ontario, Canada Email: [email protected]

Daniel Jeanmonod Department of Functional Neurosurgery, University Hospital Zu¨rich, Zu¨rich, Switzerland Email: [email protected]

Yves Keravel Service de Neurochirurgie, Hoˆpital Henri Mondor, Cre´teil, France

Fiacro Jime´nez Epilepsy Surgery Clinic; Unit for Stereotactic, Functional Neurosurgery and Radiosurgery, General Hospital of Mexico City, Mexico

Sadaquate Khan Institute of Neurosciences, Frenchay Hospital, Bristol BS16 1LE, UK Deepak Khuntia Department of Human Oncology, University of

xxxvii

xxxviii

List of contributors

Wisconsin, 600 Highland Ave, K4-B100, Madison, WI, USA Email: [email protected]

Paul Kongkham Division of Neurosurgery, Toronto Western Hospital and University of Toronto, Toronto, Canada

Jong-Hyun Kim Fellow in Neurosurgery, Department of Neurosurgery, 600 North Wolfe Street, Meyer 8–181, Baltimore, MD 21287, USA Email: [email protected]

Peter Konrad Director of Functional Neurosurgery, Vanderbilt University Medical Center, Department of Neurological Surgery, Rm T–4224; MCN, 37232–2380, Nashville, Tennessee, USA Email: [email protected]

James A. J. King Sick kids Hospital, 555 University Avenue, M5G 1X8, Toronto, Ontario, Canada Zelma H. T. Kiss Associate Professor, Neurosurgery University of Calgary, Calgary, Alberta T2N 4N1, Canada Email: [email protected] Nancy E. Klipfel Department of Pathology, Keck School of Medicine University of Southern California, GNH 2900, 1200 North State St., CA, USA Email: [email protected] Kazu Kobayashi Fellow in Neurosurgery, Department of Neurosurgery, 600 North Wolfe Street, Meyer 8–181, Baltimore, MD 21287, USA Martin Kocher Professor, Department of Radiation Oncology, University Hospital, 50924 Cologne, Germany Douglas Kondziolka The Departments of Neurological Surgery, and Radiation Oncology, The University of Pittsburgh, PA, USA The Center for Image-Guided Neurosurgery, University of Pittsburgh Medical Center, Pittsburgh, PA 15213, USA E-mail: [email protected]

Brian Harris Kopell Medical School of Wisconsin, 8701 Watertown Plank Road, WI 53226, Milwaukee, USA Email: [email protected] Brenda Kosaka Division of Neurosciences, University of British Columbia, 2329 West Mall, V6T 1Z4, Vancouver, Canada Paul Krack Joseph Fourier University, Pavillon B - Grenoble University Hospital, 38700, Grenoble, France Joachim K. Krauss Chairman and Director, Department of Neurosurgery, Medical University, MHH CarlNeuberg-Str. 1, 30625 Hannover, Germany Email [email protected] S. A. Kuhn Ames Associate (Smart Systems and Nanotechnology), NASA Ames Research Center, CA 94035, Moffett Field, USA Ron Kupers PET Unit & Department of Surgical Pathophysiology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark Email: [email protected]

List of contributors

Ruben Kuzniecky Professor, NYU Comprehensive Epilepsy Center, Department of Neurology, New York University Medical Center, NY, USA Email: [email protected] Lauri V. Laitinen Unit of Functional Neurosurgery, Institute of Neurology, Box 146, Queen Square, WC1N 3BG, London, UK Martine L. M. Lamfers Department of Neurosurgery, Erasmus Medical Center, Rotterdam, The Netherlands Anthony E. Lang Division of Patient Based Clinical Research, Toronto Western Hospital McLaughlin Pavilion, 7th Floor Rm 7–403, 399 Bathurst Street, M5T 2S8, Toronto, Ontario, Canada Email: [email protected] Edward R. Laws Department of Neurosurgery, University of Virginia, Box 800212, HSC, VA, 22908–0212, Charlottesville, USA Email: [email protected] Adrian Laxton Division of Neurosurgery, Toronto Western Hospital, University of Toronto, UHN, Toronto, Ontario, Canada Yves Lazorthes Service de Neurochirurgie, Hospital LarreyRangueil, Avenue Jean Poulhes, 31403, Toulouse, France Email: [email protected] Jean Franc¸ois LeBas Joseph Fourier University, Pavillon B - Grenoble University Hospital, 38700, Grenoble, France

Dominique Leduc IREENA, Faculte´ des Sciences de Nantes, Nantes, France Foo-Chiang Lee Consultant Neurosurgeon, Division of Neuroscience Sunway Medical Center, No. 5 Jln Lagoon Selatan, Bandar Sunway, 46150, Selangor, Subang Jaya, Malaysia Email: [email protected] Dan Leksell Lars Leksell Professor of Neurological Surgery, University of Pittsburgh, B400 UPMC, Pittsburgh, PA 15213, USA Frederick A. Lenz Professor of Neurosurgery, The Johns Hopkins University School of Medicine, Department of Neurosurgery, 600 North Wolfe Street, Meyer 8–181, Baltimore, MD 21287, USA Email: [email protected] M. Leone Department of Neurosurgery, Neurological Institute Foundation “C. Besta”, Milan, Italy Marc Levivier Department of Neurosurgery, CHUV, and Centre Universitaire Romand de Neurochirurgie, Lausanne, Switzerland Email: [email protected] J. Li Ames Associate (Smart Systems and Nanotechnology), NASA Ames Research Center, CA 94035, Moffett Field, USA Go¨ran Lind Department of Neurosurgery, Karolinska Institutet and Karolinska University Hospital Stockholm, Sweden

xxxix

xl

List of contributors

Bengt Linderoth Department of Neurosurgery, Karolinska University Hospital, SE 171–76 Stockholm, Sweden Email: [email protected]

John A. Lucas Associate Professor of Psychology, Mayo Clinic College of Medicine, 4500 San Pablo Rd, FL 32224, Jacksonville, USA

Christer Lindquist Director, Gamma Knife Centre, Cromwell Hospital, London, England

L. Dade Lunsford Department of Neurological Surgery, Suit B–400, University of Pittsburgh Medical Center, 200 Lothrop Street, Pittsburgh, PA 15213, USA Email: [email protected]

Andreas A. Linninger Associate Professor of Chemical Engineering and Bioengineering, University of Illinois at Chicago, Laboratory for Product and Process Design, M/C 063, 851 S. Morgan St. - 218 SEO, Chicago, Illinois 60607–7000, USA Email: [email protected]

Hans O. Lu¨ders Department of Neurology, Cleveland Clinic, 9500 Euclid Ave, OH 44195, Cleveland, USA Email: [email protected]

Nir Lipsman Division of Neurosurgery, Toronto Western Hospital, University Health Network, University of Toronto, Toronto, Ontario, Canada

Kelly E. Lyons University of Kansas Medical Center, Department of Neurology, 3599 Rainbow Blvd, Mailstop 2012, Kansas City, KS 66160, USA Email: [email protected]

Jay S. Loeffler Department of Radiation Oncology, Massachusetts General Hospital, 55 Fruit Street, MA 02114, Boston, USA Email: [email protected]

Lijun Ma Department of Radiation Oncology, University of California-San Francisco, 505 Parnassus Avenue, CA 94143–0226, San Francisco, USA

G. Lopez Movement Disorders, Functional Neurosurgery and Neurophysiology Units, Centro Internacional de Restauracion Neurologica (CIREN), Havana, Cuba

Mohammad Maarouf Department of Stereotactic and Functional Neurosurgery, University Hospital, 50924 Cologne, Germany

Andrew Losiniecki Department of Neurosurgery, University of Cincinnati College of Medicine, Cincinnati, OH, USA

Andre G. Machado Center for Neurological Restoration, Department of Neurosurgery, Department of Biomedical Engineering, Cleveland Clinic, Cleveland, OH, USA

Andres M. Lozano Division of Neurosurgery, Department of Surgery, Toronto Western Hospital, University of Toronto, 399 Bathurst Street, Toronto, Ontario, Canada Email: [email protected]

R. Macias Movement Disorders, Functional Neurosurgery and Neurophysiology Units, Centro Internacional de Restauracion Neurologica (CIREN), Havana, Cuba

List of contributors

Marcella A. Madera University of Cincinnati, Department of Neurosurgery, Cincinnati, Ohio, USA

MMC 96, 420 E. Delaware St., MN 554455–0374, Minneapolis, USA Email: [email protected]

Deepak Madhavan Department of Neurological Sciences, University of Nebraska Medical Center, Omaha, NE, USA Email: [email protected]

Ian E. McCutcheon Department of Neurosurgery, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Blvd., Box 44, Houston, Texas 77030–4009, USA Email: [email protected]

George Mandybur The Neuroscience Institute: Department of Neurosurgery, University of Cincinnati College of Medicine and Mayfield Clinic, Cincinnati, OH, USA Email: [email protected] Pirjo Manninen Department of Anesthesia, Toronto Western Hospital, 399 Bathurst Street, Toronto, Ontario, Canada Email: [email protected] Miguel Manrique Division of Neurosurgery, Clinica Universitaria, Universidad de Navarra, Centro de Investigacio´n Medica Aplicada. CIMA, Pamplona, Spain Andrea Marlowe Department of Otolaryngology, Head & Neck Surgery, The Johns Hopkins School of Medicine, Baltimore, USA C. Marras Department of Neurosurgery, Neurological Institute Foundation “C. Besta”, Milan, Italy Antonio G. Martins Ninan T. Mathew Houston Headache Clinic, Houston, Texas, USA Email: [email protected] Robert Maxwell Department of Neurosurgery, Univ of Minnesota/S.E.

Lee McDurmont Division of Neurosurgery, Department of Surgery, Saint Louis University School of Medicine, Saint Louis, Missouri, USA Mario Meglio Istituto di Neurochirurgia, Policlinico Agostino Gemelli, Lg Gemelli, 00168, Roma, Italy Email: [email protected] Minesh P. Mehta Department of Human Oncology, University of Wisconsin, 600 Highland Ave, K4-B100, Madison, WI 53792, USA Email: [email protected] Ivar Mendez Departments of Anatomy & Neurobiology and Surgery (Neurosurgery), Dalhousie University, Halifax, Nova Scotia, Canada Fang-Gang Meng Center for Functional Neurosurgery (BMS), Shanghai Jiao Tong University Ruijin Hospital and Department of Functional Neurosurgery (JGZ,KZ, FGM), Beijing Tiantan Hospital, People’s Republic of China Patrick Mertens Department of Neurosurgery, Hopital Neurologique P. Wertheimer, University of Lyon, 59 Bd Pinel, F–69003 Lyon, France

xli

xlii

List of contributors

G. Messina Department of Neurosurgery, Neurological Institute Foundation “C. Besta”, Milan, Italy

Nadim Nasr Department of Neurosurgery and Radiation Medicine, Georgetown University Hospital, 3800 Reservoir Rd, 20007, Washington DC, USA

Bjo¨rn A. Meyerson Department of Neurosurgery, Karolinska Institute and Karolinska University Hospital Stockholm, Stockholm, Sweden Email: [email protected]

Jules M. Nazzaro University of Kansas Medical Center, Department of Neurology, 3599 Rainbow Blvd, Mailstop 2012, Kansas City, KS 66160, USA

John Mitrofanis University of New South Wales, Australia

Mary B. Newman Department of Neurosurgery, Rush University Medical Center, Chicago, IL, USA

Alon Y. Mogilner Section of Functional and Restorative Neurosurgery, North Shore-LIJ Health System, Manhasset, New York, USA Anne Morel Department of Functional Neurosurgery, University Hospital Zu¨rich, Zu¨rich, Switzerland Alexander Muacevic European CyberKnife™ Center Munich, Max Lebsche Platz 31, 81377 Munich, Germany Email: [email protected] Debabrada Mukherjee Department of Neurosurgery, Toronto Western Hospital, 399 Bathurst Street, M5T 2S8, Toronto, Canada Karim Mukhida Cell Restoration Laboratory, Room 12H1, Departments of Anatomy & Neurobiology and Surgery (Neurosurgery), Dalhousie University, 5850 College Street, Halifax, Nova Scotia, Canada B3H 1X5 Email: [email protected] Dipankar Nandi Imperial College London and Charing Cross Hospital, London, UK

Michael E. Newmark Kelsey-Seybold Clinic, 2727 W. Holcombe Blvd, 2nd floor Neurology, TX 77025, Houston, USA Email: [email protected] Jean Paul Nguyen Department of neurosciences, CHU Laennec, Nantes, France Email: [email protected] John K. Niparko Department of Otolaryngology, Head & Neck Surgery, The Johns Hopkins School of Medicine, Baltimore, USA Email: [email protected] Ajay Niranjan The Departments of Neurological Surgery, and Radiation Oncology, The University of Pittsburgh, PA, USA The Center for Image-Guided Neurosurgery, University of Pittsburgh Medical Center, Pittsburgh, PA 15213, USA Soheyl Noachtar Department of Neurology, Cleveland Clinic, 9500 Euclid Ave, OH 44195, Cleveland, USA Josef Novotny The Departments of Neurological Surgery, and

List of contributors

Radiation Oncology, The University of Pittsburgh, PA, USA The Center for Image-Guided Neurosurgery, University of Pittsburgh Medical Center, Pittsburgh, PA 15213, USA Wieslaw L. Nowinski Biomedical Imaging Lab, Agency for Science, Technology & Research (ASTAR), 30 Biopolis Street, 138671, The Matrix, Singapore Email: [email protected] Jose´ Marı´a Nu´n˜ez Epilepsy Surgery Clinic; Unit for Stereotactic, Functional Neurosurgery and Radiosurgery, General Hospital of Mexico City, Mexico Bart Nuttin Department of Neurosurgery, University Hospital Gasthuisberg and Katholieke Universiteit Leuven, Herestraat 49, B–3000, Leuven, Belgium Email: [email protected] Jose A. Obeso Department of Neurology and Neurosurgery, Clinica Universitaria and Medical School and Neuroscience Division, CIMA Centro de Investigacio´n Biome´dica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), University of Navarra, Pamplona, Spain Email: [email protected] Michael Y. Oh Assistant Professor of Neurosurgery, Drexel University College of Medicine Co-Director, Division of Neuromodulation Department of Neurosurgery, Allegheny General Hospital, 420 East North Ave, PA 15212, Pittsburgh, USA Email: [email protected] Chihiro Ohye Functional & Gamma Knife Surgery Center, 886

Nakao-machi, 370–0001, Takasaki, Gunma, Japan Email: [email protected] George Ojemann Department of Neurological Surgery RI–20, University of Washington Medical Center, Campus Box 356470, 1959 N.E. Pacific Street, WA 98195, Seattle, USA Email: [email protected] David Omahen Department of Neurosurgery, Toronto Western Hospital, 399 Bathurst Street, M5T 2S8, Toronto, Canada Hiroshi Otsubo Division of Neurology, Department of Pediatrics, The Hospital for Sick Children, University of Toronto, 555 University Avenue, Toronto, Ontario, M5G 1X8, Canada Email: [email protected] Alondra Oubre´ Department of Neurosurgery, North Shore University Hospital, 9 Tower, Manhassett, NY 11030, USA Jorge Roberto Pagura Centro Integrado de Dor, Rua Baltazar da Veiga 490, S.P. 04510, Sao Paolo, Brazil Email: [email protected] Rajesh Pahwa University of Kansas Medical Center, Department of Neurology, 3599 Rainbow Blvd, Mailstop 2012, Kansas City, KS 66160, USA Kamalakannan Palanichamy Massachusetts General Hospital, Department of Radiation Oncology, Cox 3, 100 Blossom Street, Boston, MA 02114, USA

xliii

xliv

List of contributors

Stephan Palfi Service de Neurochirurgie, Hoˆpital Henri Mondor, Cre´teil, France Michael C. Park Department of Clinical Neurosciences, Program in Neurosurgery, The Warren Alpert Medical School of Brown University, Rhode Island Hospital, Providence, RI 02903, USA E-mail: [email protected] Erik C. Parker Department of Neurological Surgery, NYU School of Medicine, 530 First Ave, Suite 8R, NY, USA Andrew G. Parrent Department of Clinical Neurosciences, University Hospital, 339 Windemere Rd., N6A 5A5, London, Ontario, Canada Email: [email protected] Nikunj K. Patel Institute of Neurosciences, Frenchay Hospital, Bristol BS16 1LE, UK N. Pavon Movement Disorders, Functional Neurosurgery and Neurophysiology Units, Centro Internacional de Restauracion Neurologica (CIREN), Havana, Cuba Richard D. Penn Professor of Neurosurgery, The University of Chicago Medical Center Section of Neurosurgery, MC 3026 5841 South Maryland Avenue, Chicago, Illinois 60637, USA E-mail: [email protected] Erlick A. C. Pereira Oxford Functional Neurosurgery, Nuffield Department of Surgery, University of Oxford and Department of Neurological Surgery, The West Wing, The John Radcliffe Hospital, Oxford, OX3 9DU, UK Email: [email protected]

Roland Peyron CHU de Saint-Etienne & INSERM U879, University of St. Etienne, Lyon, France Email: [email protected] Brigitte Piallat Joseph Fourier University, Pavillon B - Grenoble University Hospital, 38700, Grenoble, France Julie G. Pilitsis Assistant Professor, University of Massachusetts, School of Medicine, Worcester, MA, USA Email: [email protected] Puneet Plaha Institute of Neurosciences, Frenchay Hospital, Bristol BS16 1LE, UK Bernd Pohlmann-Eden Bethel Epilepsy Centre, Bielefeld, Germany Epilepsy Service, Division of Neurology, Dalhousie University, Halifax, Canada Pierre Pollak Joseph Fourier University, Pavillon B - Grenoble University Hospital, 38700, Grenoble, France Kumar M. Prakash Division of Patient Based Clinical Research, Toronto Western Hospital McLaughlin Pavilion, 7th Floor Rm 7–403, 399 Bathurst Street, M5T 2S8, Toronto, Ontario, Canada Arthur Prochazka Department of Physiology and Centre for Neuroscience, University of Alberta, Edmonton AB T6G 2S2, Canada Jean Quint Oropilla Consultant in Neurosurgery, Makati Medical Center, Philippines Email: [email protected]

List of contributors

Peter Rabins John Hopkins Hospital, Meyer 279, 600 N. Wolfe St., 21287–7279, MD, Baltimore, USA Email: [email protected] Sylvie Raoul Service de Neurochirurgie, Hoˆpital G. et R. Lae¨nnec, Bd J. Monod, 44093 NANTES cedex, France Email: [email protected] Stig Rehncrona Lunds Universitet, Box 117, SE-221 00 Lund, Sweden Email: [email protected] R. Reichart Ames Associate (Smart Systems and Nanotechnology), NASA Ames Research Center, CA 94035, Moffett Field, USA Ali Rezai Director, Center for Neurological Restoration, Jane and Lee Seidman Chair in Functional Neurosurgery, Department of Neurosurgery, Cleveland Clinic, Cleveland, OH, USA Email: [email protected]

H. Ian Robins Department of Medicine and Human Oncology, University of Wisconsin, 600 Highland Ave, K4-B100, Madison, WI 53792, USA Email: [email protected] M. C. Rodriguez-Oroz Department of Neurology and Neurosurgery, Clinica Universitaria and Medical School and Neuroscience Division, CIMA Centro de Investigacio´n Biome´dica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), University of Navarra, Pamplona, Spain R. Rodriguez-Rojas Movement Disorders, Functional Neurosurgery and Neurophysiology Units, Centro Internacional de Restauracion Neurologica (CIREN), Havana, Cuba Robert Rosenwasser Department of Neurosurgery, Thomas Jefferson University Hospital, Philadelphia, PA, USA V. Roualdes Department of neurosciences, CHU Laennec, Nantes, France

Donald Richardson Emeritus Professor Neurosurgery, Tulane University Health Science Center, New Orleans, Louisiana, USA Email: [email protected]

James T. Rutka Division of Neurosurgery, Suite 1503, The Hospital for Sick Children, 555 University Avenue, Toronto, Ontario, Canada M5G 1X8 Email: [email protected]

R. Mark Richardson Department of Neurological Surgery, University of California, San Francisco, 505 Panassus Ave, Box 0112, CA, USA

Tejas Sankar Department of Neurosurgery, Lahey Clinic Medical Center, Tufts University School of Medicine, Boston, Massachusetts, USA

David W. Roberts Section of Neurosurgery, Dartmouth Medical School, Hannover, NH 03755, USA Email: [email protected]

Raymond Sawaya Department of Neurosurgery - 442, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Blvd., Houston, TX 77030, USA Email: [email protected]

xlv

xlvi

List of contributors

David W. Schaal Clinical Development, Accuray Incorporated, Sunnyvale, CA, USA Nicholas D. Schiff Department of Neurology and Neuroscience, Weill Medical College of Cornell University, 1300 York Avenue Room F610, New York, New York, 10021, USA Email: [email protected] David Schlesinger Lars Leksell Center for Gamma Surgery, Department of Neurosurgery, University of Virginia, Charlottesville, VA, USA Michael Schulder Department of Neurosurgery, North Shore University Hospital, 9 Tower, Manhassett, NY 11030, USA Email: [email protected] Theodore H. Schwartz Department of Neurological Surgery, Weill Medical College of Cornell University, New YorkPresbyterian Hospital, New York, NY, USA Gunnar Sedin University of Uppsala, Uppsala, Sweden Email: [email protected]

Helen A. Shih Departments of Radiation Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA Email: [email protected] Jay L. Shils Department of Neurosurgery, Lahey Clinic, 41 Mall Road, 01805, Burlington, MA, USA Email: [email protected] Dennis C. Shrieve Department of Radiation Oncology, Massachusetts General Hospital, 55 Fruit Street, MA 02114, Boston, USA Email: [email protected] Marc P. Sindou Chairman Department of Neurosurgery, University Claude-Bernard of Lyon Hoˆpital Neurologique Pierre Wertheimer, 59 Bd Pinel, 69677, BRON CEDEX, France Email: [email protected] V.A. Sironi Fondazione Istituto Neurologico, “C. Besta”, Milan, Italy

Eric Seigneuret Joseph Fourier University, Pavillon B - Grenoble University Hospital, 38700, Grenoble, France

Michelle J. Smith Department of Neurological Surgery, Weill Cornell Medical College, New York, NY, USA

Jason P. Sheehan Box 800–212, Department of Neurological Surgery, Health Sciences Center, Charlottesville, VA 22908, USA

Penny K. Sneed Department of Radiation Oncology, University of California-San Francisco, 505 Parnassus Avenue, CA 94143–0226, San Francisco, USA Email: [email protected]

Andrew G. Shetter Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona 85013, USA Email: [email protected]

Brian Snyder Division of Neurosurgery, Toronto Western Hospital, University of Toronto, UHN, Toronto, Ontario, Canada

List of contributors

J. C. Sol Multidisciplinary Pain Center Unit of Stereotactic and Functional Neurosurgery, Department of Neuroscience, University Hospital of Toulouse, Toulouse, France Jens Christian Sørensen Department of Neurosurgery, Aarhus University Hospital, DK–8000 Aarhus C, Denmark Philip A. Starr Department of Neurological Surgery, University of California, San Francisco, USA Email: [email protected] Richard B. Stein Department of Physiology and Centre for Neuroscience, University of Alberta, Edmonton AB T6G 2S2, Canada Email: [email protected] Ladislau Steiner Lars Leksell Center for Gamma Surgery, Department of Neurosurgery, University of Virginia, Charlottesville, VA, USA Email: [email protected] Melita Steiner Lars Leksell Center for Gamma Surgery, Department of Neurosurgery, University of Virginia, Charlottesville, VA, USA Scellig Stone Division of Neurosurgery, Department of Surgery, Toronto Western Hospital, University of Toronto, Toronto, Ontario, Canada A. P. Strafella PET Imaging Centre, Center of Addiction Mental Health, University of Toronto, Toronto, Ontario, Canada Movement Disorders Center, Toronto Western Hospital & Research Institute, University of Toronto,

Toronto, Ontario, Canada Email: [email protected] Volker Sturm Professor, Department of Stereotactic and Functional Neurosurgery, University Hospital, 50924 Cologne, Germany Email: [email protected] Bomin Sun Center for Functional Neurosurgery (BMS), Shanghai Jiao Tong University Ruijin Hospital and Department of Functional Neurosurgery (JGZ,KZ,FGM), Beijing Tiantan Hospital, People’s Republic of China Peter Tai Epilepsy Program, Toronto Western Hospital, University of Toronto, Toronto, Canada Takaomi Taira Director of Stereotactic and Functional Neurosurgery, Department of Neurosurgery, Tokyo Women’s Medical University, 8–1 Kawada, Shinjuku, Tokyo 1628666, Japan Email: [email protected] Mandeep Tamber Division of Neurosurgery, Toronto Western Hospital and University of Toronto, Toronto, Canada Eng-King Tan National Neuroscience Institute, Singapore General Hospital, Singapore Farzana Tariq Department of Neurosurgery, Brigham and Women’s Hospital, 75 Francis St, Boston, MA 02115, USA Daniel Tarsy Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, USA

xlvii

xlviii

List of contributors

Ronald R. Tasker Department of Physiology, University of Toronto, 1 King’s College Circle, M5S 1S8, Toronto, Canada Ethan Taub Oberarzt, Department of Neurosurgery, Basel University Hospital, Spitalstrasse 21, CH–4031 Basel, Switzerland Email: [email protected] Michael D. Taylor Sick Kids Hospital, 555 University Avenue, M5G 1X8, Toronto, Ontario, Canada Email: [email protected] Manoel Jacobsen Teixeira Division of Functional Neurosurgery, University of Sa˜o Paulo Medical School, Rua Mena Barreto 765 - Itaim Bibi, SP- 014033–010, Sa˜o Paulo, Brazil Email: [email protected]

Ohio, USA Email: [email protected] Napoleon Torres Joseph Fourier University, Pavillon B - Grenoble University Hospital, 38700, Grenoble, France Zulma Tovar-Spinoza Division of Neurosurgery, Suite 1503, The Hospital for Sick Children, 555 University Avenue, Toronto, Ontario, Canada M5G 1X8 David Trejo Epilepsy Surgery Clinic; Unit for Stereotactic, Functional Neurosurgery and Radiosurgery, General Hospital of Mexico City, Mexico Wen-Ching Tzaan Department of Neurosurgery, Chang Gung Medical College and Memorial Hospital, 5 Zu Shung St., Kweishan, Taoynan 333, Taiwan

Carlos R. Telles-Ribeiro Neurodor - Neurosurgery and Pain Clinic, Rua Visconde de Piraja 351/509, Cep: 22471–002, Ipanema, Rio de Janeiro, RJ, Brazil Email: [email protected]

Ryan J. Uitti Mayo Clinic College of Medicine, 4500 San Pablo Rd, FL 32224, Jacksonville, USA

David G. T. Thomas Division of Neurosurgery, The National Hospital for Neurology & Neurosurgery, Queen Square, Box 32, WC1N 3BG, London, UK

Taufik A. Valiante Univeristy of Toronto, Department of Surgery, CoDirector, Epilepsy Program, Krembil Neuroscience Center, UHN, 399 Bathurst Street 4W–436, Toronto, Ontario, Canada, M4S3H6 Email: [email protected]

Daniel Roy Thomas Department of Neurological Sciences, Christian Medical College, Vellore, Tamil Nadu 632004, India Stavropoula Tjoumakaris Department of Neurosurgery, Thomas Jefferson University Hospital, Philadelphia, PA, USA William D. Tobler Department of Neurosurgery, University of Cincinnati College of Medicine, ML 0515, Cincinnati,

T. van Eimeren PET Imaging Centre, Center of Addiction Mental Health, University of Toronto, Toronto, Ontario, Canada Kris van Kuyck Department of Neurosurgery, Laboratory of Experimental Neurosurgery and Neuroanatomy, Katholieke Universiteit Leuven, Belgium

List of contributors

X. A. Vasques CHRU Montpellier, Service de Neurochirurgie, Universite´ Montpellier I, Montpellier, France

Ana Luisa Velasco Cerrada Bosques de Moctezuma 55, La Herradura Huixquilucan, Estado de Me´xico 52780, Me´xico Email: [email protected] Francisco Velasco Epilepsy Surgery Clinic; Unit for Stereotactic, Functional Neurosurgery and Radiosurgery, General Hospital of Mexico City, Mexico Email: [email protected]

Jerrold L. Vitek Department of Neurosciences, Cleveland Clinic Foundation, 9500 Euclid Ave, NC30, Cleveland, OH 44195, USA Email: [email protected] Valerie Voon NINDS/NIH, 10 Center Dr, 20892–1428, Bethesda, Maryland, USA Email: [email protected] Juhn A. Wada Division of Neurosciences, University of British Columbia, 2329 West Mall, V6T 1Z4, Vancouver, Canada Email: [email protected]

Marcos Velasco Epilepsy Surgery Clinic; Unit for Stereotactic, Functional Neurosurgery and Radiosurgery, General Hospital of Mexico City, Mexico

J. Walter Ames Associate (Smart Systems and Nanotechnology), NASA Ames Research Center, CA 94035, Moffett Field, USA

J. C. Verdie Multidisciplinary Pain Center Unit of Stereotactic and Functional Neurosurgery, Department of Neuroscience, University Hospital of Toulouse, France

Richard Wennberg Department of Neurosurgery, Toronto Western Hospital, 399 Bathurst Street, M5S 2T8, Toronto, Ontario, Canada Email: [email protected]

Jean-Guy Villemure Director, Division of Neurosurgery, University of Montreal, Professor and Chairman, Neurosurgery Service, Centre hospitalier de l’universite´ de Montre´al, 1560 Sherbrooke East, Montreal, Canada H2L 4M1 Email: [email protected]

Karin N. Westlund Marine Biomedical Institute, University of Texas Medical Branch, 2925 Beluche, TX 77551, Galveston, USA

Veerle Visser-Vandewalle Department of Neurosurgery, Academic Hospital Maastricht, P.O. Box 5800, 6202, AZ Maastricht, The Netherlands Email: [email protected]

Robert E. Wharen, Jr. Mayo Clinic College of Medicine, 4500 San Pablo Rd, FL 32224, Jacksonville, USA Email: [email protected] Edward White Institute of Neurosciences, Frenchay Hospital, Bristol BS16 1LE, UK

xlix

l

List of contributors

Donald M. Whiting Drexel University College of Medicine Director, Division of Neuromodulation Vice-Chairman, Department of Neurosurgery, Allegheny General Hospital, 420 East North Ave, PA 15212, Pittsburgh, USA Thomas Wichmann Department of Neurology, Emory University Woodruff Memorial Research Building 101 Woodruff Circle, Atlanta, GA 30322, USA Heinz Gregor Wieser Neurology Department, University Hospital Zurich, Frauenklinikstrasse 26, 8091 Zurich, Switzerland Email: [email protected] William D. Willis, Jr. Marine Biomedical Institute, University of Texas Medical Branch, 2925 Beluche, TX 77551, Galveston, USA Email: [email protected] Shiao Y. Woo The University of Texas MD Anderson Cancer Center, Proton Therapy Center- Houston, 1840 Old Spanish Trail, TX 77054, Houston, USA Email: [email protected] Isaac Yang Department of Neurological Surgery, University of California San Francisco, USA Email: [email protected] Je´roˆme Yelnik INSERM U679, Hoˆpital de la Salpeˆtrie`re, 47, Bd de

l’Hoˆpital, 75013, Paris, France Email: [email protected] Chun-Po Yen Lars Leksell Center for Gamma Surgery, Department of Neurosurgery, University of Virginia, Charlottesville, VA, USA Jianguo Zhang Center for Functional Neurosurgery (BMS), Shanghai Jiao Tong University Ruijin Hospital and Department of Functional Neurosurgery (JGZ,KZ, FGM), Beijing Tiantan Hospital, People’s Republic of China Kai Zhang Center for Functional Neurosurgery (BMS), Shanghai Jiao Tong University Ruijin Hospital and Department of Functional Neurosurgery (JGZ,KZ, FGM), Beijing Tiantan Hospital, People’s Republic of China Ludvic U. Zrinzo Division of Neurosurgery, The National Hospital for Neurology & Neurosurgery, Queen Square, Box 32, WC1N 3BG, London, UK Email: [email protected] Dominik Zumsteg Neurology Department, University Hospital Zurich, Frauenklinikstrasse 26, 8091 Zurich, Switzerland

7 A Brief History of Stereotactic Neurosurgery in Switzerland E. Taub

Though he was not a neurosurgeon, the first great stereotactician in Switzerland was surely Walter Rudolf Hess (1881–1973), Professor of Physiology at the University of Zurich from 1917 to 1951. From the 1920s onward, he performed basic studies on the functional organization of the diencephalon, using electrical stimulation through stereotactically implanted depth electrodes in freely moving cats [1]. For this work, he was given the Nobel Prize in Physiology or Medicine in 1949, sharing the award with Anto´nio Egas Moniz (1874–1955), the Portuguese inventor of leukotomy and of cerebral angiography. Hugo Krayenbu¨hl (1902–1985), who had been trained as a neurosurgeon by Sir Hugh Cairns in London, became Professor of Neurosurgery in Zurich in 1948 – the first such chair in the country. He was active in functional neurosurgery from the beginning, publishing a study of prefrontal leukotomy and topectomy for the treatment of pain in 1950 [2] and a case series of temporal cortical excision and lobectomy for epilepsy in 1953 [3]. It is reported that he performed the first stereotactic procedures in Switzerland in 1958, in collaboration with Mehmet Gazi Yas¸argil, operating with a Riechert frame [4]. (It was, of course, Yas¸argil who was to succeed Krayenbu¨hl as chief of neurosurgery upon his retirement in 1973). In these early years of functional (lesional) stereotaxy, Krayenbu¨hl and Yas¸argil used equipment designed by their Zurich physiologist colleague O. A. M. Wyss [5] to perform both thalamotomies and #

Springer-Verlag Berlin/Heidelberg 2009

pallidotomies for the treatment of Parkinson’s disease and other extrapyramidal disorders [6]. In the 1960s, functional and stereotactic neurosurgery in Krayenbu¨hl’s department became the domain of Jean Siegfried, who had developed his interests in the field as a Fellow under William H. Sweet at Massachusetts General Hospital in 1962. In the late 1960s, Siegfried wrote on percutaneous cordotomy and the surgical treatment of spasmodic torticollis and proposed stereotactic dentatotomy for the treatment of movement disorders [7,8,9]. Toward the end of the decade, with the introduction of L-DOPA, Siegfried took on the question of medical versus surgical treatment of Parkinson’s disease, writing extensively on the subject and gaining a very large clinical experience in stereotactic lesionmaking [10]. At the same time, he became Switzerland’s leading expert in Sweet’s technique of radiofrequency thermocoagulation of the Gasserian ganglion for the treatment of trigeminal neuralgia, eventually amassing a huge case series: a report on the first 500 cases, published in 1977, was followed by a report on 1,000 cases in 1981 [11,12]. Siegfried went on to become a pioneer of deep brain stimulation and one of the prime movers in the transformation of functional neurosurgery – now nearly, though not entirely, complete – from a ‘‘lesioning’’ to a ‘‘stimulating’’ discipline. He stimulated the sensory thalamus for the treatment of chronic pain in a series of 89 patients from 1978 to 1985 [13] and began to perform thalamic stimulation for tremor in the

74

7

A brief history of stereotactic neurosurgery in switzerland

late 1980s [14]. After the reintroduction of pallidotomy by Laitinen and colleagues in the early 1990s, Siegfried was the first to describe the achievement of comparable effects by pallidal stimulation [15]. After Siegfried’s move from the University across the Lake of Zurich to the Klinik Im Park (originally called AMI Klinik Im Park), a private clinic that had been opened in 1986, he also had the distinction of introducing Gamma Knife radiosurgery to Switzerland. He founded the Gamma Knife Center at the Klinik Im Park in 1994 and headed it until his retirement in 2001. Siegfried’s activities at the Klinik Im Park were continued by Thomas Mindermann (2000-present) and Ethan Taub (2001– 2007), a former fellow of Ronald Tasker and Andres Lozano at the University of Toronto. Epilepsy surgery had already been an interest of Krayenbu¨hl’s in the 1950s, as mentioned above, and was further developed in Zurich by both Siegfried and Yas¸argil. In 1970, Siegfried and the epileptologist Christoph Bernoulli brought the technique of stereoencephalography (SEEG) for the localization of epileptic discharges to Zurich, 5 years after its description by Bancaud and Talairach in Paris [16]. In the early 1980s, together with the epileptologist Heinz Gregor Wieser, Yas¸argil pioneered the technique of selective amygdalohippocampectomy for the treatment of mesiobasal limbic epilepsy [17]. At around the same time, SEEG gave way to semi-invasive localization via foramen ovale electrodes, which were first described by Siegfried, Wieser, and H. R. Stodieck [18]. From 1993 onward, the Zurich tradition of selective amygdalohippocampectomy was continued by Yas¸argil’s successor as chairman, Yasuhiro Yonekawa. Also at the University of Zurich, Daniel Jeanmonod has headed the Laboratory for Functional Neurosurgery for some years, continuing into the present. Known in the clinical sphere as one of the few current proponents of deep brain lesioning, as opposed to stimulation, he has pursued basic research on the pathophysiology of

movement disorders and other neurological conditions. His research group has published a detailed stereotactic atlas of the thalamus [19]. Off to the west, in the French-speaking part of Switzerland, both epilepsy surgery and functional stereotaxy became major areas of clinical activity in Lausanne after Jean-Guy Villemure moved there from the Montreal Neurological Institute to become chairman in 1997. Villemure’s department achieved high case numbers and became a renowned center of excellence in both areas. In particular, he and his group amassed a large series of patients who underwent subthalamic stimulation for Parkinson’s disease and published very important findings about both the usefulness of this procedure and its complications [20,21]. After Villemure’s retirement in 2006, his activities in the functional field were continued by his disciples Jocelyne Bloch and Claudio Pollo under his successor as chairman, Marc Levivier. Joachim-Kurt Krauss, currently chief of neurosurgery at the Medizinische Hochschule in Hanover (Germany), briefly headed the functional neurosurgery unit at the University of Berne in the 1990s. He was succeeded in this capacity (1999–2001) by Ethan Taub, who later brought deep brain stimulation procedures to Basel (2007present) in collaboration with Morten Wasner. Deep brain stimulation in Berne is currently the responsibility of Alexander Stibal. Heinz Fankhauser began a deep brain stimulation program at the private Clinique Cecil in Lausanne in 2002, while Ronald Bauer, a former fellow of Tipu Aziz at Oxford, has led the functional neurosurgery unit at the Cantonal Hospital in St. Gallen since 2006. The current state of functional neurosurgery in Switzerland can thus be briefly summarized: There are active clinical programs in deep brain stimulation at the University Hospitals of Lausanne, Berne, and Basel, as well as at the Cantonal Hospital in St. Gallen and at a private clinic in Lausanne. The Gamma Knife Center at the Klinik Im Park, long the only dedicated facility for stereotactic radiosurgery

A brief history of stereotactic neurosurgery in switzerland

in Switzerland, is still in operation as of this writing and is likely to be joined by other centers in this field in the near future. Across the country, scientific presentations for the medical public and articles in the lay press are gradually heightening awareness of the uses of functional neurosurgery among referring physicians and prospective patients, and activity in the field can be expected to expand and to flourish.

References 1. Hess WR. Die funktionelle Organisation des vegetativen Nervensystems. Basel: Schwabe; 1948. 2. Krayenbu¨hl H, Stoll W. [Prefrontal leucotomy and topectomy for the treatment of irreducible pain]. Rev Neurol (Paris) 1950;83(1):40-1. 3. Krayenbu¨hl H, Hess R, Weber G. [Electroencephalographic, corticographic, and surgical considerations on 21 cases of temporal epilepsy treated by cortical excision and lobectomy]. Rev Neurol (Paris) 1953;88(6):564-7. 4. Siegfried J, quoted in Nashold BS. The history of stereotactic neurosurgery. Stereotact Funct Neurosurg 1994;62:29-40. 5. Wyss OAM. Hochfrequenzkoagulationsgera¨t zur reizlosen Ausschaltung. Helv Physiol Pharmacol Acta 1945;3:437-43. 6. Krayenbu¨hl H, Wyss OAM, Yas¸argil MG. Bilateral thalamotomy and pallidotomy as treatment for bilateral Parkinsonism. J Neurosurg 1961;18:429-44. 7. Siegfried J. [Percutaneous cordotomy]. Schweiz Med Wochenschr 1967;97(40):1325-6. 8. Siegfried J. [Surgery for spasmodic torticollis]. Schweiz Med Wochenschr 1967;97(40):1325. 9. Siegfried J, Perret E. [Stereotaxic dentatotomy. New method of surgical treatment of hyperkinesis]. Rev Otoneuroophtalmol 1968;40:(7)341-3.

7

10. Krayenbu¨hl H, Siegfried J. [Treatment of Parkinson’s disease: L-dopa or stereotaxic technics?]. Neurochirurgie 1970;16(1):71-6. 11. Siegfried J. 500 Percutaneous thermocoagulations of the Gasserian ganglion for trigeminal pain. Surg Neurol 1977;8(2):126-31. 12. Siegfried J. Percutaneous controlled thermocoagulation of Gasserian ganglion in trigeminal neuralgia: experiences with 1000 cases. In: Samii M, Jannetta P, editor. The cranial nerves. Berlin: Springer; 1981. p. 322-30. 13. Siegfried J. Sensory thalamic neurostimulation for chronic pain. Pacing Clin Electrophysiol 1987;10(1 Pt 2):209-12. 14. Blond S, Siegfried J. Thalamic stimulation for the treatment of tremor and other movement disorders. Acta Neurochir Suppl (Wien) 1991;52:109-11. 15. Siegfried J, Lippitz B. Bilateral chronic electrostimulation of ventroposterolateral pallidum: a new therapeutic approach for alleviating all parkinsonian symptoms. Neurosurgery 1994;35(6):1126-9. 16. Lu¨ders H, Comair YG, (eds). Epilepsy surgery. 2nd ed. Philadelphia, PA: Lippincott Williams and Wilkins; 2000. p. 48. 17. Wieser HG, Yas¸argil MG. Selective amygdalohippocampectomy as a surgical treatment of mesiobasal limbic epilepsy. Surg Neurol 1982;17(6):445-57. 18. Siegfried J, Wieser HG, Stodieck SR. Foramen ovale electrodes: a new technique enabling presurgical evaluation of patients with mesiobasal temporal lobe seizures. Appl Neurophysiol 1985;48(1–6):408-17. 19. Morel A, Magnin M, Jeanmonod D. Multiarchitectonic and stereotactic atlas of the human thalamus. J Comp Neurol 1997;387(4):588-630. 20. Vingerhoets FJ, Villemure JG, Temperli P, Pollo C, Pralong E, Ghika J. Subthalamic DBS replaces levodopa in Parkinson’s disease: two-year follow-up. Neurology 2002;58(3):396-401. 21. Burkhard PR, Vingerhoets FJ, Berney A, Bogousslavsky J, Villemure JG, Ghika J. Suicide after successful deep brain stimulation for movement disorders. Neurology 2004;63(11):2170-2.

75

16 History of Stereotactic and Functional Neurosurgery in Brazil O. Vilela Filho

When Andres Lozano invited me to write this chapter, although honored, I declined the invitation at first. After all, very little had been written about this issue. The neurosurgeon Sebastia˜o Gusma˜o, the person who has most studied the history of Brazilian neurosurgery, has already written a significant number of papers about this subject, but basically nothing about the history of the Brazilian stereotactic and functional neurosurgery. Therefore, being the president of the Brazilian Society for Stereotactic and Functional Neurosurgery, I felt impelled to accept the challenge and write this chapter, but not without some extra pressure from Lozano. It was a tough job. I called and emailed colleagues throughout this country innumerable times, at any time, and I suppose they must be tired of me, obviously not without reason. In the case of colleagues already dead, their relatives, friends and colleagues were my target. Not very infrequently, the same fact was presented with different versions, obliging me to dig even deeper. But here it comes at last, the first paper on this issue. I have done my very best and, I must say, it truly fascinated me. If any incongruity has occurred, it was not my fault, since most of the times I had to base myself on told stories instead of recorded information. Dear editors and friends, please accept my apologies for having missed the deadline so many times. The beginning of the history of Brazilian general and functional neurosurgery is closely intermingled, being humanly impossible to separate them, and that is how I decided to start this chapter. #

Springer-Verlag Berlin/Heidelberg 2009

A Brief History of Brazilian Neurosurgery and the First Functional Procedures Performed in Brazil According to Horrax [1], the history of neurosurgery in modern times may be divided into three periods: pre-Lister (1710–1846), preHorsley (1846–1890), and modern neurosurgery (from 1890 until today). The first known neurosurgical procedure performed in Brazil was carried out by the surgeon Luis Gomes Ferreyra, in 1710, in the vicinities of Sabara´, a town located in the countryside of Minas Gerais State. The patient was a slave presenting with a compound depressed skull fracture caused by the natural fall of a tree branch. Ferreyra removed the bone fragments, performed hemostasis using silk threads from cobwebs soaked in egg white, and covered the bone defect with a piece of calabash shell until bone healing. The patient eventually recovered and returned to work, presenting as only sequel a very mild expression dysphasia [2]. The pre-Horsley period started with the clinical introduction of general anesthesia by Morton, in 1846, and of antisepsis by Lister, in 1867. In Brazil, differently from Europe, this period extended until 1928. During this phase, neurosurgical interventions were almost completely limited to the treatment of depressed skull fractures and drainage of extracerebral hematomas and abscesses [2,3].

198

16

History of stereotactic and functional neurosurgery in brazil

Curiously, many functional procedures were started in Brazil in the end of the pre-Horsley period. Following are the pioneers of some of these operations [3]. Paolo Josetti, in 1896, performed a gasserian ganglion resection for the treatment of trigeminal neuralgia. In 1903, Joa˜o Burnier and Jose´ Hungria Jr performed periarterial sympathectomy for the treatment of causalgia. Paes Leme, in an imprecise date, but certainly before 1910, carried out the first surgical procedure for epilepsy in a patient presenting with Jacksonian seizures, starting in the right hemiface, caused by encephalomalacia of the central part of the left middle frontal gyrus, which was secondary to head injury and subsequent brain abscess. In 1913, Nascimento Gurgel employed peripheral neurectomies (Stoffel’s technique) to treat spasticity. From this period, worth mentioning was the contribution from Augusto Paulino de Souza and Ame´rico Vale´rio [3]. At that time, the prevalent idea was that the entire rolandic area (pre- and postcentral gyri) was related to motor control. In 1907, these surgeons operated on a victim from cranial missile wound presenting with contralateral hemiplegia. During the operation, being the brain widely exposed through a large craniectomy, they observed the complete integrity of the posterior rolandic area (postcentral gyrus). Based on this surgical finding, they hypothesized that the posterior rolandic area was not involved in motor control. This hypothesis, presented at the Fourth Latin American Medical Congress, held in Rio de Janeiro in 1909, and mentioned in the 1922 paper of the authors [3], was confirmed by Horsley, Campbell, and Dana 2 years later (1909). The above mentioned authors, among many others, are considered the predecessors of neurosurgery in our country [2]. Two surgeons are regarded as the precursors of Brazilian neurosurgery: Augusto Branda˜o Filho, known as the prince of the surgeons, and Alfredo Monteiro, another formidable general

surgeon, both from Rio de Janeiro, at that time the capital of the country [2]. Branda˜o Filho, in 1924, was the first to perform ventriculography in Brazil, and on 6 August 1928, directly supervised by Egas Moniz, he performed the first cerebral angiography in the Americas, in fact, only 14 months after Egas Moniz, assisted by Almeida Lima, invented this procedure (28 June 1927) [2]. Branda˜o Filho also performed some open cordotomies (according to Jose´ Portugal), two gasserian ganglion resections for trigeminal neuralgia (though the first patient died, an excellent result was achieved in the second), as well as brain tumor resection in seven patients, all of which died according to his publication of 1931 [2]. Noteworthy is the fact that the initial experimental researches performed by Egas Moniz and Almeida Lima that culminated with the development of human cerebral angiography were carried out at Instituto Rocha Cabral, in Lisbon. This institute was founded and maintained by the Portuguese Bento da Rocha Cabral, greatuncle of one of the most important Brazilian neurosurgeons, still very active, Guilherme Cabral, from Belo Horizonte, capital of Minas Gerais State [2]. In 1928, Antoˆnio Austrege´silo Rodrigues Lima, an eminent neurologist and the first Professor of Neurology in Brazil (1912, Federal University of Rio de Janeiro, as it is called today), visited many neurosurgical services in USA, including those headed by Cushing, Dandy, Adson, and Frazier, and was very impressed with what he saw. Back to Brazil, he urged the brilliant and very skillful general surgeon, Alfredo Monteiro, and his young and recently graduated (1927) assistant, Jose´ Ribe Portugal, to start neurosurgery in Brazil. To do so, he inaugurated the Neurosurgical Service of the Department of Neurology of Federal University of Rio de Janeiro (Universidade Federal do Rio de Janeiro – UFRJ). In 1932, this service became a department, and Alfredo Monteiro was

History of stereotactic and functional neurosurgery in brazil

invested its head and the first Professor of Neurosurgery in Brazil. In 1935, Monteiro, under his own request, was transferred to the Department of Operative Techniques and Experimental Surgery, and Portugal, stimulated by his former boss, took over the chair of Neurosurgery [2]. In the early 1930s, both Branda˜o Filho and Alfredo Monteiro, probably disenchanted with their results, mainly in brain tumor operations, and realizing that surgery of the nervous system should be performed by people with adequate knowledge and formation in neurological sciences, including anatomy, pathophysiology, semiology, neurology, and neurosurgical techniques, that is, by true neurosurgeons, decided to abandon neurosurgery. They really never considered themselves as neurosurgeons, but general surgeons performing neurosurgery [2]. For the reasons aforementioned, Antoˆnio Austrege´silo Rodrigues Lima may be regarded as the godfather of Brazilian neurosurgery. The inauguration of modern neurosurgery in the world, in 1890, was led by the association of the following essential technological innovations: general anesthesia, antisepsis, Broca’s theory of cerebral localization (further corroborated and enlarged by the findings of Jackson, Fritsch & Hitzig, and Ferrier) and the studies on cranioencephalic topography carried out by Broca (still very important, but even more in a time when neuroimaging studies were not available) [2]. In the late 1920s, being neurosurgery well established in the world, neurology and general surgery well developed in Brazil, and considering the fact that state-of-the-art neuroimaging techniques (ventriculography and cerebral angiography) had already been introduced in the country, the moment was favorable for the birth of modern neurosurgery in Brazil [2]. Modern Brazilian neurosurgery was then inaugurated [2], having as pioneers Jose´ Ribe Portugal (1901–1992) and Elyseu Paglioli

16

(1898–1985), and in our opinion, also Antoˆnio Carlos Gama Rodrigues, or Carlos Gama (1904– 1963), as he was known. All of them started neurosurgery in their respective states, Rio de Janeiro, Rio Grande do Sul, and Sa˜o Paulo, approximately at the same time. Jose´ Portugal and Carlos Gama were, initially, self-taught, and just sometime later in their carriers they visited the services of the icons of world neurosurgery. Portugal, in 1945, spent 4 months with John Scarff, in New York, returning in 1947 for 6 more months. Gama, on the other hand, visited the service of Harvey Cushing. Differently, Elyseu Paglioli only started his neurosurgical practice after spending 8 months in Paris (1930) with De Martel, one of the pioneers of French neurosurgery [2]. Elyseu Paglioli and Jose´ Portugal founded two of the most important Brazilian neurosurgical schools. Of interest for this chapter, Paglioli formed Manoel Krimberg, one of the beginners of stereotactic and functional neurosurgery in Rio Grande do Sul State, and Djacir Figueiredo, the pioneer of stereotactic and functional neurosurgery in Ceara´ State. From Portugal’s school emerged Renato Barbosa, regarded as the pioneer of stereotactic and functional neurosurgery in Brazil, Gianni Temponi, another very well known Brazilian functional neurosurgeon, and Joffre Lima, the beginner of stereotactic and functional neurosurgery in Para´ State. Carlos Gama did not found a neurosurgical school, but he did form Rolando Tenuto, who headed the Neurosurgical Service at the University of Sa˜o Paulo (Universidade de Sa˜o Paulo – USP) Medical School teaching hospital (Clinic Hospital) from its inauguration, in 1945, until his retirement, in 1970, having formed, among many others, Jose´ Zaclis, one of the pioneers in stereotactic and functional neurosurgery in Sa˜o Paulo State, and Raul Marino Jr, the most widely known Brazilian functional neurosurgeon; this service became also one of the most important Brazilian neurosurgical schools [2].

199

200

16

History of stereotactic and functional neurosurgery in brazil

The Brazilian Society of Neurosurgery (Sociedade Brasileira de Neurocirurgia – SBN) was founded by the twelve Brazilian neurosurgeons that attended the First International Congress of Neurological Surgeons in Brussels, Belgium, on 26 July 1957 [2], and became affiliated to the World Federation of Neurosurgical Societies in the same year. Jose´ Portugal and Elyseu Paglioli were among the twelve founding members, and were elected, respectively, the first and third president of the SBN. Both were later reelected for another term. According to the last census, performed in 2005, there are currently 2,251 neurosurgeons in Brazil, 1,735 of which are members of the SBN, making it the third in the world in number of members [2]. Interestingly, the three pioneers of neurosurgery in Brazil were in some way involved with functional neurosurgery, making relevant contributions to the field. Graduated from medical school in 1927, 2 years later Jose´ Portugal underwent examination for full professorship of the Department of Surgical Techniques and Experimental Surgery, Medical School, Federal University of Rio de Janeiro, occasion in which he presented the thesis entitled Contribuic¸a˜o a` Neurectomia Retrogasseriana (Contribution to Retrogasserian Neurectomy). This work was itself already a register of his main contributions to the field. His interest in the surgical treatment of trigeminal neuralgia, in fact, started during the last 3 years (total duration of medical school, including internship: 6 years) of his medical school, when he was a monitor of Anatomy (in the Brazilian university system, the monitor is a student who helps teaching a discipline he/she has already attended; to get this academic position, those interested should undergo an examination, when the best candidate is chosen), and remained his primary interest throughout his whole carrier. He was really a superb neurosurgeon [2]. According to Mario Brock, one of his disciples, Portugal used to perform a retrogasserian neurectomy in

roughly 20 min [4]. This procedure was so perfected by him that, in 1938, Leriche, the pioneer of pain surgery, came to Rio de Janeiro to observe one of his operations [2]. Regarding his contributions to the field of functional neurosurgery, the first one was registered when he was still a medical student and monitor of Anatomy. At that time, the prevailing idea, as shown in the first edition of Hovelaque’s book, was that the motor root of the trigeminal nerve crossed the gasserian ganglion though its outer aspect and joined the mandibular division of the trigeminal nerve externally. While making an anatomical preparation of the Fifth cranial nerve, however, Portugal noted that its motor root crossed the gasserian ganglion through its middle part and joined the mandibular division internally. Puzzled with this finding, which was in contradiction with the ‘‘bible’’ of Anatomy, he dissected many other specimens, confirming his initial observation. His findings were published in 1926, and again in 1929, being cited in Rouviere’s Anatomy [2]. His second contribution was in regard to the relative distribution of the three divisions of the trigeminal nerve in its sensory root. According to Stookey, the lateral, intermediate and medial parts of the trigeminal sensory root corresponded, respectively, to V3, V2 and V1. Portugal, however, showed that the entire external half of the sensory root corresponded to V3, and that the preservation of the medial 1/5 of the sensory root was enough to maintain corneal innervation and so prevent keratitis and consequent visual loss [2]. Finally, the third and most important contribution from Portugal to this field was the original clinical introduction of intradural retrogasserian neurectomy for the treatment of trigeminal neuralgia (1929) in a time when everybody else used the extradural approach [2]. Carlos Gama was also very fond of trigeminal procedures. In 1929 he improved the technique of gasserian ganglion alcoholization and published his first papers on this subject. Later, in 1938, Gama became Professor of the Department

History of stereotactic and functional neurosurgery in brazil

of Neurology at the USP Medical School presenting his thesis entitled Neuralgias do Trigeˆmeo (Trigeminal Neuralgias) [2]. Elyseu Paglioli was a neurosurgeon of many publications, two of which are of particular interest to the field of functional neurosurgery. The first was the thesis Circulac¸a˜o Venosa dos Nu´cleos Centrais do Ce´rebro (Venous Circulation of the Basal Ganglia), which was presented in 1927 to secure the chair of Anatomy at the Federal University of Rio Grande do Sul, and published in 1929 [2]. The second was the thesis entitled Ventriculografia (Ventriculography), prefaced by his former chief, De Martel, and presented in 1938 to obtain the chair of Surgical Clinic at the Federal University of Rio Grande do Sul Medical School [2]. The apex of his stupendous academic carrier was reached in 1950, when he became the dean of the university, a position he occupied for twelve consecutive years. Besides his neurosurgical and academic carriers, he was also engaged in politics, being mayor of Porto Alegre, the capital of Rio Grande do Sul State, and Minister of Health during the administration of the Brazilian President Joa˜o Goulart [2].

Stereotactic and Functional Neurosurgery in Brazil: From Early Days to Present Time Brazil is a large country, the fifth in the world in extension. It is divided into 26 states and the federal district, which are agrouped in five regions: North, Northeast, Midwest, Southeast, and South. For didatical reasons, we decided to describe the history of stereotactic and functional neurosurgery in Brazil considering its different regions.

Southeast Region The Southeast region is made up by the states of Rio de Janeiro, Sa˜o Paulo, Minas Gerais, and Espı´rito Santo.

16

It is hard to ascertain who the pioneer of stereotactic and functional neurosurgery in the Southeast and in Brazil was. It depends on a number of parameters not clearly defined, but certainly one of the following will fulfill the criteria: Renato Tavares Barbosa, Paulo Niemeyer, both from Rio de Janeiro, or Aloysio Mattos Pimenta, from Sa˜o Paulo.

Rio de Janeiro State Renato Tavares Barbosa (1912–2003) (> Figure 16-1) graduated from the Federal University of Minas Gerais Medical School. After that, he went to Rio de Janeiro, being the first disciple formed by Jose´ Portugal, pioneer of Brazilian neurosurgery. Initially, he worked as an assistant to Portugal [2]. In the 1950s, Barbosa went to Freiburg, Germany, where he got his training in stereotactic and functional neurosurgery with Riechert and Mundinger [5]. His first stereotactic operation was performed at Rio de Janeiro Neurological Institute, Federal University of Rio de Janeiro, . Figure 16-1 Renato Barbosa

201

202

16

History of stereotactic and functional neurosurgery in brazil

in 1958, using the Riechert and Mundinger apparatus [2]. Throughout his life he accumulated a huge experience with stereotactic treatment of movement disorders, mainly Parkinson’s disease, and psychosurgery (open procedures such as prefrontal leucotomy and cingulectomy), initially at Rio de Janeiro Neurological Institute, and later at Lagoa Hospital, where he was head of the Neurosurgery Service for 27 years, and at Sorocaba Clinic, a private hospital. According to Luiz Fernando Martins, in 1971, at that time doing his internship at Lagoa Hospital, Barbosa was the first in Brazil to use a radiofrequency generator to perform thermocoagulation lesions. Until then, thermocoagulation lesions were made by using electrocautery: placing the stethoscope on the skull, one could ‘‘hear’’ the lesion being produced, which was stopped when tremor arrest was achieved or side effects started to appear. He was one of the founders of the Brazilian Society of Neurosurgery, being elected its president for the biennium 1970/1972 [2]. He was also one of the founders of Brazilian Society for Stereotactic and Functional Neurosurgery (1980), becoming its first president [6]. Renato Barbosa, one of the pioneers of stereotactic and functional neurosurgery in our country, was the first to dedicate most of his practice to this field, which he did during his whole career. For these reasons, he is regarded as the father of Brazilian stereotactic and functional neurosurgery [2]. Paulo Niemeyer (1914–2004) (> Figure 16-2), brother of the worldwide known architect, Oscar Niemeyer (a 100 years old and still very active, the planner of the most important buildings in Brası´lia, remarried his 60-year-old secretary when he was already 98) and father of Paulo Niemeyer Filho, at present one of the most renowned Brazilian neurosurgeons, was actually the first to perform stereotactic surgery in Brazil. Niemeyer graduated from the Federal University of Rio de Janeiro Medical School in 1936. His initial training was in general surgery, which he did under the supervision of Augusto Paulino,

. Figure 16-2 Paulo Niemeyer

Professor of Surgery and Head of the Surgical Clinic at Santa Casa de Miserico´rdia do Rio de Janeiro Hospital (at that time the teaching hospital of the Federal University of Rio de Janeiro Medical School), and Alfredo Monteiro, Professor of the Department of Operative Techniques and Experimental Surgery at the same institution and one of the precursors of Brazilian neurosurgery [2,7,8]. His interest in neurosurgery became apparent in 1939, when he started dedicating to the surgery of head injury, until then part of the general surgery practice [2,7]. At the beginning a self-taught neurosurgeon, just like Jose´ Portugal, later on he visited important and well-established neurosurgical centers of other countries [2]. Since 1943 he became interested in functional neurosurgery, particularly in the surgical treatment of movement disorders and epilepsy [2,7,8]. Before the stereotactic era, he treated many patients harboring Parkinson’s disease, athetosis

History of stereotactic and functional neurosurgery in brazil

and other hyperkinesias employing pyramidotomy or cortical resection [7,9], and on 14 April 1954, he performed the first stereotactic surgery (left pallidotomy for PD in a 60-year-old patient) in South America, using the frame he was given by Riechert [7]. The report of his experience with stereotactic treatment of dyskinesias was the first publication of this kind in South America [10]. According to Niemeyer, when he was still an 8-year-old child, while alone with his beloved sister, Judith, she presented a seizure, the first of a series to follow. It was this event that later led him to Medicine, in general, and to epilepsy surgery, in particular [8]. In 1946 he was the first to perform electrocorticography in Brazil [7]. Initially, he used this technique in an attempt to demonstrate, in humans, the existence of cortical spreading depression, as previously reported in animals by Aristides Lea˜o, a Brazilian scientist [7,8,11]. The paper derived from this research was widely recognized. Subsequently, he used not only electrocorticography, but also electrographic exploration with implanted electrodes, to determine epileptic foci [7,8]. In 1949, together with the neurologist Abraham Ackerman, he founded the Brazilian League Against Epilepsy [2,7,8]. Some meetings on epilepsy and electrocorticography were then organized. The French epileptologist Henri Gastaut was invited for two of these meetings (1954 and 1955). During his lectures, Gastaut showed evidence suggesting the involvement of amygdala and hippocampus in the genesis of temporal lobe epilepsy. At that time already experienced with Falconer’s en bloc temporal lobectomy technique (26 cases), Niemeyer, in 1956, inspired by Gastaut’s findings, was the first in the world to perform selective amygdalo-hippocampectomy for treating temporal lobe epilepsy. He approached the mesial temporal structures through a 2-cm incision placed in the second temporal gyrus, and named his technique transventricular amygdalohippocampectomy [2,7,8,12].

16

Recommended by Paul Bucy, he was invited by the Department of Health, Education, and Welfare of the American Government to participate in the Second International Colloquium on Temporal Lobe Epilepsy, in Washington, organized by the National Institute of Neurological Diseases and Blindnesses, in 1957, to show his technique, which was published in the following year [7,8,12]. Another important contribution from Niemeyer was his original observation that immediately after selective amygdalo-hippocampectomy, the abnormal cortical activity, as shown by pre-resection electrocorticography, becomes surprisingly worse, and that this abnormality subsides in a few days, as demonstrated through electrodes left in the subdural space [8,12]. This finding was reported in his 1958 paper [12]. More recently, two Brazilians, during their fellowship at Montreal Neurological Institute, the epileptologist Fernando Cendes and the epilepsy surgeon Arthur Cukiert, came to the same conclusion and called the aforementioned phenomenon ‘‘Niemeyer’s effect’’ [13]. In 1953, Niemeyer became head of the Department of Neurosurgery of Santa Casa de Miserico´rdia do Rio de Janeiro Hospital [7]. In 1957, he was among the 12 Brazilian neurosurgeons that founded the Brazilian Society of Neurosurgery [2]. In 1981, in Munich, he was elected second Vice-President of the World Federation of Neurosurgical Societies (WFNS), and in 1997, in Netherlands, he received the Honor Medal of the WFNS, which was awarded to five living neurosurgeons of the world that most contributed for the progress of neurosurgery [7]. The single thing he was most proud of, though, was the large number of neurosurgeons that he trained, now spread all over the country [7]. After 1958, unfortunately, his interest in functional neurosurgery progressively declined, and he became dedicated almost exclusively to general neurosurgery, in particular to microsurgery for

203

204

16

History of stereotactic and functional neurosurgery in brazil

intracranial aneurisms and transesphenoidal approach for pituitary tumors [2,7]. On 10 March 2004, Paulo Niemeyer passed away [7,8]. Undoubtedly, a great loss to Brazilian and World neurosurgery. Gianni Maure´lio Temponi (1934–2007), another pioneer of stereotactic and functional neurosurgery in Brazil, graduated from the Federal University of Triaˆngulo Mineiro Medical School in 1959 [2,14]. His neurosurgical training (1961/1964) was carried out at Rio de Janeiro Neurological Institute under Jose´ Portugal. Renato Barbosa was the functional neurosurgeon in charge at the same institution, and it was from him that he got his training in stereotactic and functional neurosurgery. When Barbosa moved to Lagoa Hospital, Temponi was left in charge of functional neurosurgery. Posteriorly, he became Director of Rio de Janeiro Neurological Institute, Full Professor of Neurosurgery at Federal University of Rio de Janeiro Medical School (1972), and founded the Neurosurgical Service at Clementino Fraga Filho Hospital, the teaching hospital at Federal University of Rio de Janeiro. As head of the Service, he formed 45 neurosurgeons. Like his master in stereotactic and functional neurosurgery, Renato Barbosa, his main areas of interest were stereotactic treatment of movement disorders and psychosurgery. During his career, always using the Riechert and Mundinger apparatus, Temponi performed 478 ventriculographyguided procedures, mainly thalamotomy for Parkinson’s disease [15], dentatotomy for cerebral palsy (dystonia, chorea and spasticity), the theme of his PhD thesis defended in 1971 (‘‘Stereoencephalotomy for cerebral palsy in children’’), and psychosurgery (especially for heretic oligophrenia). He was so confident and satisfied with his results that, contrarily to almost everyone else, he never replaced ventriculography with computed tomography and/or magnetic resonance imaging as a tool for determining the stereotactic coordinates of functional targets. Temponi left four offspring, two of

them (Vicente and Gianni) neurosurgeons in Rio de Janeiro. Carlos Roberto Telles Ribeiro or simply Carlos Telles (> Figure 16-3), as he is known, is certainly one of the most respected and renowned functional neurosurgeons in the country nowadays. Telles graduated from the State University of Rio de Janeiro Medical Sciences School in 1969. In 1973 he finished his residence training at Brası´lia District Hospital, in Brası´lia, under Paulo Mello. From 1976 to June of 1979, he stayed as a fellow at University of Hannover, doing his PhD under Wolfhard Winkelmu¨ller. Invited by Mario Brock, in July 1979 he moved to the University of Berlin, where he inaugurated the Pain Clinic and, in 1980, defended his PhD thesis, supervised by Winkelmu¨ller, entitled ‘‘Treatment of chronic pain by electrical stimulation of the spinal cord.’’ After almost 1 year in Berlin, he went to Duke University, spending 1 month with Blaine Nashold Jr. Returning to Brazil in 1980, by invitation of Pedro Sampaio, Professor of Neurosurgery and Head of the Division of Neurosurgery at

. Figure 16-3 Carlos Telles

History of stereotactic and functional neurosurgery in brazil

Pedro Ernesto Hospital, teaching hospital at the State University of Rio de Janeiro, Telles inaugurated the first multidisciplinary pain clinic in Brazil, which was probably one of his most important contributions to Brazilian stereotactic and functional neurosurgery. He was also the first to perform spinal cord stimulation for the treatment of pain in our country. Still in 1980, as will be mentioned later in this chapter, his role was fundamental for the foundation of the Brazilian Society for Stereotactic and Functional Neurosurgery. His main contribution to stereotactic and functional neurosurgery was the development of the technique he called combined solitary tractotomy (RF solitary tractotomy + RF lesioning of the subnucleus caudalis of the trigeminal nerve + C2 and C3 dorsal rhizotomy), which was performed through an open procedure, and designed to treat pain secondary to invasive cancer of the head and neck in the distribution of the V, IX and X cranial nerves and cervical region [16–18]. This technique was performed in more than 50 patients, providing excellent pain relief in 80% of them. Though never published, it was presented in three important meetings: 14th Brazilian Congress of Neurosurgery (Belo Horizonte, Brazil, 1982) [16], 20th Latin American Congress of Neurosurgery (Sa˜o Paulo, Brazil, 1983) [17], and Annual Meeting of the American Society for Stereotactic and Functional Neurosurgery (North Caroline, US, 1983) [18]. In 1991, he spent 6 months at the University of Freiburg, under Christopher Ostertag, doing his post-doctorate thesis (‘‘Stereotactic biopsy for the diagnosis of deep brain lesions’’). In 1992, after the retirement of Pedro Sampaio, he became Professor and Head of the Service of Neurosurgery at Pedro Ernesto Hospital, State University of Rio de Janeiro. Still very active, and having dedicated most of his life to the treatment of pain, he supervised the formation of more than 40 physicians in the area of pain, many of them illustrious pain specialists in our country. Other of his areas of expertise are

16

stereotactic biopsy of deep brain lesions, percutaneous cordotomy for cancer pain (> 800 cases), sympathetic procedures for the treatment of complex regional pain syndromes, DREZotomy, and trigeminal procedures (> 1,300 cases using RF retrogasserian rhizotomy, microvascular decompression, or balloon microcompression of the Gasserian ganglion). Carlos Telles was president of both the Brazilian Society for Stereotactic and Functional Neurosurgery (1988/1990) and Brazilian Society of Neurosurgery (1996/1998). Currently, there are some other colleagues in Rio de Janeiro with an impressive experience in stereotactic and functional neurosurgery, among them: Alexandre Amaral, Servidores Pu´blicos Estaduais Hospital (training with Manoel Teixeira); Ce´sar Fantezia Andrauss, Rio de Janeiro Neurological Institute (training with Gianni Temponi); Eduardo Carlos Barreto, Quinta D’Or Hospital (training with Carlos Telles and Mario Brock); Paulo L. C. Cruz, Santa Casa de Miserico´rdia do Rio de Janeiro Hospital (training with Manoel Teixeira); Ney Jose´ Monteiro, Lagoa Hospital (training with Renato Barbosa); Jose´ Augusto Nasser dos Santos, Esta´cio de Sa´ University (training at Columbia University); and Marcello Reis da Silva, Clementino Fraga Filho Hospital (training with Jean Claude Peragut). Eduardo Barreto was one of the founders of the Brazilian Chapter of the International Neuromodulation Society – Brazilian Neuromodulation Society (May 2007), occasion in which he was elected its first president. Ce´sar Andrauss, in 1997, helped by an engineer, built the TCA stereotactic apparatus, a modification of the Leksell frame; until 2005, when the last unity was built, 28 apparatuses had been manufactured by hand.

Sa˜o Paulo State Two of the pioneers in stereotactic and functional neurosurgery in Brazil are from Sa˜o Paulo State: Aloysio Mattos Pimenta and Jose´ Zaclis.

205

206

16

History of stereotactic and functional neurosurgery in brazil

Aloysio Mattos Pimenta (1912–1987) (> Figure 16-4) graduated from the University of Sa˜o Paulo (Universidade de Sa˜o Paulo – USP) Medical School in 1935. During his internship, in 1935, he divided his time between the Surgical Clinic, headed by Alves Lima; Neurological Clinic, headed by Enjolras Vampre´ (the pioneer of Neurology in Sa˜o Paulo), both at Santa Casa de Miserico´rdia de Sa˜o Paulo Hospital, at that time the teaching hospital at the USP Medical School; and Juqueri Hospital, a psychiatric institution. We assume that, since Carlos Gama, pioneer of neurosurgery in Sa˜o Paulo and Brazil, was the only neurosurgeon of the Neurological Clinic at the time, Mattos Pimenta accompanied him also. In 1936, he was part of the delegation of the USP Medical School that visited Argentina, spending most of his time with Manuel Balado, then one of the most prominent South American neurosurgeons. The combination of these different experiences, we believe, enabled Mattos Pimenta to start his neurosurgical practice [2,19]. In 1936, the same year Egas Moniz published the initial results of prefrontal leucotomy, Mattos . Figure 16-4 Aloysio Mattos Pimenta

Pimenta, oriented by Pacheco e Silva (Professor of Psychiatry at the University of Sa˜o Paulo Medical School), was one of the first in the world and the first in the Americas to perform the prefrontal leucotomy of Egas Moniz, which took place at Juqueri Hospital, in fact only a few days before Freeman and Watts performed their first psychosurgical procedure in the USA [2,19]. Until the late 1940s, assisted by the psychiatrist Mario Yahn and the neurosurgeon Afonso Sette Jr, Mattos Pimenta performed 279 operations of this type. The technique of Egas Moniz was used in the first 161 patients (before 1945), the technique proposed by Freeman and Watts in the 48 intermediate patients of their series, and the staged Freeman and Watts procedure (operation performed in three stages), as proposed by Mario Yahn, in the last 70 patients. The results obtained in the 279 patients were compiled in a book authored by Yahn, Mattos Pimenta and Sette Jr, and was prefaced by Egas Moniz and published in 1951 [20]. In August 1948, Egas Moniz chaired the First International Congress of Psychosurgery, which was held in Lisbon. During its closing session, the Brazilian delegation (Mattos Pimenta, Paulino Longo, Pacheco e Silva, Ma´rio Yahn, Anı´bal Silveira, E´lio Simo˜es, and Antoˆnio Carlos Barreto), led by Paulino Longo (head of the Neurological Division, Paulista Medical School, Federal University of Sa˜o Paulo) proposed the official nomination of Egas Moniz for the Nobel Prize considering his two great and universally accepted achievements, cerebral angiography and prefrontal leucotomy. The proposal was enthusiastically accepted and embodied by the members of the delegations of the 26 other countries that attended the meeting [2]. He had already been nominated for this award twice before, but in both occasions his nomination was declined. In 1949 Egas Moniz was at last awarded the Noble Prize in Physiology and Medicine for his invaluable contribution with the prefrontal leucotomy, no mention made, however, of his discovery of the cerebral angiography.

History of stereotactic and functional neurosurgery in brazil

At the beginning, without formal training, Mattos Pimenta performed only simpler procedures. In order to polish his neurosurgical formation, he spent 2 years (1938 and 1939) in Europe, most of the time with To¨nnis, in Berlin, but also with Zu¨lch, in Berlin (2 months), Fo¨erster, in Breslau (1 month), Olivercrona, in Stockholm (1 month), Busch, in Copenhagen, Leriche, in Strassbourg, and Clovis Vincent, in Paris. Due to the eclosion of World War II, however, he had to return to Brazil much earlier than he had planned. Always a restless creature, in January 1942 he went to the New York Neurological Institute, spending 4 months with Stookey and Putnam, and then moved on to the University of Michigan, where he stayed for 20 months under the supervision of Max Peet [2,19]. Back to Brazil, in 1944 he started working at the Neurological Clinic of Paulista Medical School, Federal University of Sa˜o Paulo, headed by Paulino Longo. In 1947, the Neurosurgical Division of this institution was officially inaugurated and Mattos Pimenta was invested its head, position that he held until his retirement (1982). In the 1960s he became Full Professor of Neurosurgery of Paulista Medical School, and in 1980 he started up the post-graduation course in neurosurgery (master degree and PhD), still the only one in the country [2,19]. Eventually he became involved with stereotactic surgery for Parkinson’s disease (PD). The date, though, is uncertain. We had the opportunity to analyze his curriculum vitae prepared in November, 1959 [19]. It is a very detailed CV, but no mention is made concerning any training in stereotactic surgery. Fernando Braga, who started his neurosurgical training under Mattos Pimenta in 1961, however, told us that his uncle, presenting with Parkinson’s disease, was operated on by his chief, who used the Riechert and Mundinger apparatus, in the same year he started his training. For this very reason, we inferred that Mattos Pimenta spent some time with Riechert and Mundinger in Freiburg in 1960, and after

16

returning to Brazil, started performing stereotactic surgery in 1961. Since then he operated on Parkinson’s disease with certain regularity for many years, but always as an appendage of his neurosurgical career. Neuro-oncology was always the apple of his eye. His associative activity was also intense. He was one of the twelve founders and the second president of Brazilian Society of Neurosurgery (1958/1959), presiding its second congress in 1959 (Campos do Jorda˜o, Sa˜o Paulo State) [2]. In 1965 he was president of the 11th Latin-America Congress of Neurosurgery, held in Sa˜o Paulo, having as official topics only stereotactic surgery and urgencies in neurosurgery [21]. Maybe even more important were his activities in the World Federation of Neurosurgical Societies: First vice-president (1973/1977), honorary president (elected in 1977), and president of its congress held in Sa˜o Paulo in 1977. Two other neurosurgeons performed stereotactic and functional neurosurgery at Sa˜o Paulo Hospital, the teaching hospital at Federal University of Sa˜o Paulo: Fernando Menezes Braga and Fernando Antonio Patriani Ferraz. Fernando Braga, once finished his training at Paulista Medical School, spent 1 year (1965/ 1966) in Edinburgh with Gillinghan, doing mostly general neurosurgery, but also some stereotactic and functional neurosurgery. Before coming back to Brazil, he purchased the McCaul apparatus, and in 1967, performed his first thalamotomy in a parkinsonian patient at Sa˜o Paulo Hospital. Along the years, mainly until 1970, he accumulated a significant experience with stereotactic treatment of movement disorders. In 1992, as Division Head and Professor of Neurosurgery, Braga entrusted Fernando Ferraz the task of creating the Stereotactic and Functional Neurosurgery Service at the Division of Neurosurgery at Federal University of Sa˜o Paulo. Ferraz, an ex-resident of the institution, already had some training in stereotactic and functional neurosurgery, which he had acquired

207

208

16

History of stereotactic and functional neurosurgery in brazil

from Mattos Pimenta and Braga. Before starting this new task, though, he went to UCLA School of Medicine and spent a short time with Antonio De Salles. A CT/MR-compatible stereotactic apparatus was acquired (Micromar stereotactic system), and then, still in 1992, the service, almost completely dedicated to the treatment of movement disorders, was finally inaugurated. Ferraz did a great job. The service went remarkably well until the beginning of the 2000s, when, due to a number of institutional problems, it faded away. It is very unfortunate, since Federal University of Sa˜o Paulo is considered one of the centers of excellence for neurosurgical training in Brazil. In this regard, it is probably wise mentioning that, just as in the case of Mattos Pimenta, stereotactic and functional neurosurgery was only an appendage of the neurosurgical practice of Braga and Ferraz. None of them was actually a functional neurosurgeon by ‘‘birth’’ and this can have made a real difference. The most important center of training in stereotactic and functional neurosurgery in Sa˜o Paulo is, in fact, the USP Medical School, which started by the hands of Jose´ Zaclis, another pioneer of the field. Graduated from the University of Sa˜o Paulo (USP) Medical School in 1944, Jose´ Zaclis (1917–1983) (> Figure 16-5a) was formed neurosurgeon by Rolando Tenuto, Professor of Neurosurgery and Head of the Division of Neurosurgery at the Clinic Hospital, teaching hospital at the USP Medical School [22]. The main assistant to Tenuto, in 1947 he was given the task of organizing the Neuroradiology Service of the institution [2,22]. From this time on, he dedicated almost exclusively to this area, performing ventriculography, pneumoencephalography, myelography, and cerebral angiography. He was the first to describe the technique of cerebral pan-angiography by means of injection of contrast medium into a single artery while simultaneously producing transient intrathoracic hypertension [23,24]. His service was the first

entirely dedicated to neuroradiology in Brazil. Since at that time stereotactic surgery relied basically on ventriculography, in which he was an expert, after a trip to Germany, Russia, and USA, places where he became acquainted with different stereotactic apparatuses, and with the help of the engineer Koralek, he built, in 1961, the HC stereotactic apparatus (HC stands for Hospital das Clı´nicas) (> Figure 16-5b) [25]. The equipment was set in a room of the neuroradiology unit completely dedicated to stereotactic surgery, where he used part of his time to perform stereotactic procedures for movement disorders and pain. The operations were carried out with the patient in a sitting position. This was the second Brazilian made stereotactic frame, in fact the first really elaborated and arc-centered apparatus. Only two of these frames were produced: one for the USP Medical School, and another for the Rio de Janeiro Neurological Institute. From 1971 to 1974, he was Head of the Division of Neurosurgery, and Professor at the USP Medical School. After Zaclis came Raul Marino Jr and Manoel Teixeira. Raul Marino Jr (> Figure 16-6) graduated from the USP Medical School in 1960, and after finishing his neurosurgical training in the same institution in 1964, under Rolando Tenuto, he went to North America to brush up his formation. In 1965, while in Boston, he divided his time between the Lahey Clinic, accompanying James Poppen and Charles Fager, who introduced him to stereotaxis and surgery for movement disorders, and the laboratory of Walle Nauta at the Massachusetts Institute of Technology (MIT), where he was for the first time really exposed to the limbic system, basal ganglia, and functional neuroanatomy. In 1966, still in Boston, he moved to the Massachusetts General Hospital (MGH), and was extremely fortunate to have as simultaneous supervisors professionals like Thomas Ballantine Jr (psychiatric surgery), William Sweet (pain surgery), and Raymond Kjellberg (surgery for movement disorders, brachytherapy, and

History of stereotactic and functional neurosurgery in brazil

16

. Figure 16-5 (a) Jose´ Zaclis (b) HC stereotactic apparatus, built by Zaclis and Koralek in 1961

. Figure 16-6 Raul Marino Jr

cyclotron radiosurgery for pituitary tumors and other endocrine diseases), all luminaries of the field of stereotactic and functional neurosurgery. Learning of Marino’s previous work on limbic system with Nauta at MIT, Ballantine Jr invited him to join his team and work on the cingulotomy project for mental illnesses and pain [26]. In 1967, this team published their pioneer paper on stereotactic anterior cingulotomy for psychiatric

disorders and pain [27]. According to Marino Jr (personal communication), in the 1965 publication of Ballantine’s group [28] on the same subject, the free-hand technique was used instead of the stereotactic technique and the number of cases was still too small. Marino spent the year of 1967 in Montreal. At Montreal Neurological Institute (MNI), McGill University, where he spent most of his time, he learned electroencephalography, electrocorticography, and the Wada test with Peter Gloor and epilepsy surgery with Theodore Rasmussen. There he had the opportunity to meet Wilder Penfield and Herbert Jasper. His free time was spent at the Notre Dame Hospital, University of Montreal, accompanying the stereotactic procedures of Claude Bertrand and the transsphenoidal surgeries of Jules Hardy, who later on became his brother-in-law. In 1968 he returned to the USA for an extra year at the National Institutes of Health (Bethesda, Maryland) supervised by Paul MacLean (lab work), the father of the limbic system, and Van Buren, at the time in charge of the stereotactic program [26]. After 4 years abroad, Marino finally returned to Brazil. In 1969, requested by Rolando Tenuto, his former chief, he resumed his work at the USP Medical School. Initially, he performed his stereotactic operations using the Zaclis’ HC apparatus. In 1971, after a substantial reform of

209

210

16

History of stereotactic and functional neurosurgery in brazil

the operating rooms and infirmaries of the Psychiatric Institute at the USP Medical School, Raul Marino inaugurated the first integrated, multidisciplinary Stereotactic and Functional Neurosurgery Service in Brazil, a service with 51 beds completely devoted to stereotactic and functional neurosurgery [26]. Well prepared as he was, he performed the most varied functional procedures, although his main interests, from the beginning until his retirement, always remained the same, that is, surgical treatment of epilepsy and psychiatric disorders, from which areas derived his most important contributions. Aiming to improve the electrophysiological investigation of refractory epilepsy, in 1972 he spent 6 months in Paris with Jean Talairach and Gabor Szikla, masters of the stereotactic electroencephalography technique [26]. Back to Brazil, a Talairach frame was acquired by his institution, finally replacing the Zaclis apparatus. A member of the American Branch of the International Society for Research in Stereoencephalotomy since its foundation (1968), in 1973, during the Sixth Symposium of the International Society in Tokyo, he became its member and was elected local Chairman of the next meeting (1977), which would be held in Sa˜o Paulo, Brazil, as a satellite meeting of that of the World Federation of Neurosurgical Societies (WFNS) [26]. Still during the Tokyo meeting, when was proposed a change in the name of the International Society, Marino suggested adding the term functional, which was accepted and the new designation became World Society for Stereotactic and Functional Neurosurgery. In 1977, during the Seventh Meeting of the World Society for Stereotactic and Functional Neurosurgery, Marino was elected Vice President of the Eighth Meeting of the World Society for Stereotactic and Functional Neurosurgery (the President elected was Jean Siegfried) and appointed member of the editorial board of the official journal of the society, Applied Neurophysiology (previously – 1938/1975 – called Confinia

Neurologica), later (1988) renamed as Stereotactic and Functional Neurosurgery, position that he held until his retirement in 2007 [26]. As a result of the 1977 meeting, the book Functional Neurosurgery, edited by Theodore Rasmussen and Raul Marino Jr, having as contributors an impressive number of outstanding functional neurosurgeons, was published in 1978 [29]. In his introductory chapter, Marino explains the reasons that led him to propose the term functional neurosurgery for this specialty, making a parallel with the bees behavior: ‘‘General neurosurgery tends to concentrate on the lesion, rather than on the symptoms, while functional neurosurgery focus on the symptoms, that is, on the abnormal functions, which are often hyperfunctional states that appear at a distance as a consequence of the primary lesion. Many specialties deal with the human brain, as many insects alight on the prairie flowers. However, only the bees know how to extract the honey. The bees alone are able to do that job and leave the flowers intact, without hurting or making them lose their freshness, allowing them to remain exactly as they were before. This is the hope and aim of functional neurosurgery’’ [29]. In 1980, Marino also played a very important role in the foundation of the Brazilian Society for Stereotactic and Functional Neurosurgery, and it was his close relationship with Blaine Nashold, who was present during this event, that enabled the Brazilian Society for Stereotactic and Functional Neurosurgery to be regarded as the Brazilian branch of World Society for Stereotactic and Functional Neurosurgery since its creation [26]. Raul Marino was elected the second President of Brazilian Society for Stereotactic and Functional Neurosurgery. Undoubtedly due to his great fondness for and expertise in psychiatric surgery, Marino also became Vice President of the International Society of Psychosurgery. In the 1980s (Raul Marino, personal communication), Marino was the first and the only (to the best of our knowledge) Brazilian neurosurgeon

History of stereotactic and functional neurosurgery in brazil

to use neural (dopaminergic cells) grafts in humans for the treatment of Parkinson’s disease. Autologous adrenal medullary grafts were attempted in three patients (Beneficeˆncia Portuguesa Hospital), but no benefit was achieved and this technique was abandoned. Homologous substantia nigra grafts derived from fetuses of legally approved abortions (pregnancy following rape) were tried in three other patients. However, soon afterwards these previously legal abortions became prohibited and the trials were terminated. In 1990, Marino became Full Professor of Neurosurgery and Chief of the Division of Neurosurgery at the USP Medical School, one of the most prestigious Brazilian schools of Medicine, position that he held until his retirement in 2007 [26]. During his years at the University (1971–2007) he helped to form a large number of neurosurgeons. In 1993, after spending some time at the Temple University (Philadelphia, USA), he inaugurated the second LINAC Radiosurgery Service in the country at Beneficeˆncia Portuguesa Hospital (Sa˜o Paulo). The first X-Knife service, although quite rudimentary, had already been installed by Jack Beraha at Oswaldo Cruz Hospital (Sa˜o Paulo) in 1983, having being closed in 1989. His most important contributions were in the areas of epilepsy surgery and psychosurgery [27,29–37]. As already mentioned, as part of Ballantine’s team, he played a very important role in the development of stereotactic anterior cingulotomy for the treatment of psychiatric disorders (major depression and obsessive-compulsive disorder) and pain, a technique he later spread in our country [27]. Concerning epilepsy surgery, his contributions were various, standing out: he was the first in Brazil to implement and diffuse the need of a multidisciplinary team to better evaluate the surgical candidates; his team was pioneer in establishing the electrophysiological parameter to determine the extension of the

16

callosotomy, that is, the disruption of bilateral synchrony of spike and wave discharges [30]; finally, Marino Jr was the first to propose and use the stereotactic callosotomy technique [31]. Raul Marino Jr was the first Brazilian neurosurgeon with formal training in stereotactic and functional neurosurgery and also the first to introduce the concept of a multidisciplinary stereotactic and functional neurosurgery team in our country. From the beginning, his career was almost completely devoted to the field of stereotactic and functional neurosurgery. Besides, he is by far the most renowned and prominent Brazilian functional neurosurgeon. For all these reasons, Marino Jr should be the one to be regarded as the real father of stereotactic and functional neurosurgery in Brazil. Graduated from the USP Medical School in 1972, Manoel Jacobsen Teixeira (> Figure 16-7a) finished his residence training in the same institution in 1976. During his training, he was for the first time exposed to stereotactic surgery by Jose´ Zaclis. Still in 1976, he spent 3 months at Goiaˆnia Neurological Institute under Luiz Fernando Martins, a pupil of Wilhelm Umbach, deepening his knowledge and practice in stereotactic and functional neurosurgery. In 1977 he went to Europe, where he stayed for more than 2 years. Initially, Teixeira spent 1 year and a half in Edinburgh with Edward Hitchcock, his most beloved chief and icon. Afterwards, he moved on to Zurich, spending 3 months with Jean Siegfried, and then, finally, to Freiburg, where he accompanied Mundinger during 4 months. During his outstanding career, he has visited a number of other functional neurosurgery services around the world. Teixeira started working at the Division of Neurosurgery of the Department of Neurology at the USP Medical School in 1984. In 1985, he obtained his master degree, and in 1990, his PhD. From 1997 to 2004, he was Technical Director of the Health Service of the Division of Functional Neurosurgery of the Institute of

211

212

16

History of stereotactic and functional neurosurgery in brazil

. Figure 16-7 (a) Manoel Teixeira (b) Micromar stereotactic system, model TM-03B

Psychiatry at the USP Medical School, and since 2004 he became Technical Director of the Division of Functional Neurosurgery. In March 2007, after the retirement of Raul Marino, there was an examination for full professorship in neurosurgery at the USP Medical School, and Teixeira was approved in first place, becoming Full Professor of the discipline and Head of the Division of Neurosurgery. His academic career has been quite profitable. Teixeira and his group have published a large number of papers, book chapters and books, and presented innumerable oral abstracts and posters both in national and international meetings, the vast majority in the area of pain. The multidisciplinary Pain Clinic of USP Medical School, which he runs, is most probably the busiest pain center in the country. Along the years he has formed a large number of functional neurosurgeons and pain specialists not only from Brazil but also from many other South American countries. Manoel Teixeira is a very versatile functional neurosurgeon, being experienced in all areas of the field, including brachytherapy and radiosurgery; his expertise in epilepsy and psychiatric disorders surgery, however, is less impressive. But the apple of his eye is really pain, anything in this area, from pathophysiology to the most

refined surgical technique. In fact, he is regarded by many as a living encyclopedia in this field. Also, he is certainly one of the most experienced active pain surgeons in the world. Accordingly, his most important contributions were on the surgical treatment of pain. A disciple of Edward Hitchcock, he probably is the still active neurosurgeon with the largest experience in medullary stereotactic trigeminal nucleotractotomy [38,39], a technique developed by Hitchcock in 1970 [40]. Hitchcock and Teixeira, in 1987, described the technique of pontine stereotactic trigeminal nucleotractotomy, indicated in cases of deafferentation extending through a long distance in the trigeminal nuclear complex, when the pain can not be adequately alleviated by medullary tractotomy alone [38,41]. In 2005, his group showed in rats that the motor cortex presents an antinociceptive function even under physiological circumstances and that motor cortex stimulation-induced analgesia is mediated by the opioid system [42]; for this research, Erich Fonoff received the Young Investigator Award from the World Society for Stereotactic and Functional Neurosurgery [43]. Teixeira et al., in 2007, demonstrated that the deafferentation pain associated with actinic brachial plexopathy and trigeminal neuropathy, usually unresponsive to

History of stereotactic and functional neurosurgery in brazil

various therapeutic approaches, both conservative and surgical, can be successfully relieved by, respectively, cervical DREZotomy and stereotactic trigeminal nucleotractotomy [44]. Also in 2007, using transcranial magnetic stimulation to map the motor cortex, Teixeira et al demonstrated that the response to motor cortex stimulation in patients harboring neuropathic pain secondary to brachial plexus avulsion could be predicted by the size of the field of representation of the deafferented limb in the motor cortex, being the result good or excellent in patients with larger fields and poor in those with smaller or undetectable fields; this research was awarded the NeuPSIG Poster Prize (category: clinical studies) during the Second International Congress on Neuropathic Pain (Berlin, June, 2007) [45]. Recently, his group proposed a technique for stereotactic disconnection of the hypothalamic hamartoma and so preventing gelastic and secondary seizures and aggressive behavior [46], and phrenic nerve stimulation for the treatment of refractory singultus [47]. Other important but unpublished contributions from his group were the use of computer-assisted stereotactic fenestration of aqueductal cysts for the treatment of hydrocephalus [48] and the stereotactic intracavitary instillation of amphotericin B through an indwelling catheter to treat deep intracerebral paracoccidioidomycosis cysts [49]. In our opinion, these are the most relevant contributions from Teixeira and his group, among others [50–58]. A great amount of the development of stereotactic and functional neurosurgery in our country was due to the integrated actions of Teixeira and the neurosurgical industry. In 1985, Teixeira and the engineer Antoˆnio Martos, CEO of Micromar, built the first commercially available Brazilian stereotactic apparatus, the Micromar stereotactic system, model TM-01B (Teixeira & Martos), a modification of that of Hitchcock’s. Continuous refinement led to the production of new versions of the first frame,

16

the models TM-02B, in 1991, and TM-03B, in 1996 (> Figure 16-7b). In 1998, Teixeira, Martos and the physicist Armando Alaminos produced the first linear accelerator- compatible radiosurgery system in Brazil, the Micromar radiosurgery system. Manoel Teixeira, a very well known and admired functional neurosurgeon in our country, was president of the Brazilian Society for Stereotactic and Functional Neurosurgery for two terms: 1990/1992 and 1998/2000. Other important names of stereotactic and functional neurosurgery in Sa˜o Paulo State are Jorge Roberto Pagura, Jose´ Oswaldo Oliveira Jr, Cla´udio Fernandes Correˆa, Arthur Cukiert, Jack Beraha, and Nilton Luis Latuf. Jorge Roberto Pagura (> Figure 16-8) graduated from the ABC Medical School in 1974. Once finished his neurosurgical residence (1975/1978) at Nove de Julho Hospital, in Sa˜o Paulo, under the supervision of Gilberto Machado de Almeida (also Professor of Neurosurgery and Head of the Division of Neurosurgery at the USP Medical School), he went to . Figure 16-8 Jorge Pagura

213

214

16

History of stereotactic and functional neurosurgery in brazil

Germany, where he spent 15 months (1978/1979) with Wolfhard Winkelmu¨ller at the University of Hannover. In 1980 Pagura returned to Hannover and stayed with Majid Samii for 1 month; at that time, Peter Janetta was also there showing his technique of neurovascular decompression for trigeminal neuralgia. This procedure became the one he is most fond of. In 1983 he obtained his PhD with the thesis entitled ‘‘Percutaneous radiofrequency spinal rhizotomy’’ at the Paulista Medical School, Federal University of Sa˜o Paulo, which was later published [59]. In the same year, he went to Duke University where he spent 40 days with Blaine Nashold learning the DREZ procedure. In 1996 Pagura became Full Professor and Head of the Division of Neurosurgery at ABC Medical School. His main areas of expertise are trigeminal neurovascular decompression [60], percutaneous radiofrequency glossopharyngeal rhizotomy [61], DREZotomy for pain and spasticity, and neuronavigation. His most important contributions to the literature are exactly in the two first topics above mentioned. His paper on glossopharyngeal rhizotomy, a classic in this issue, is still frequently cited [61]. Jorge Pagura was president of the Brazilian Society for Stereotactic and Functional Neurosurgery in the biennium 2002/2004. Also worth mentioning was his role in the creation of the Brazilian Society for the Study of Pain (Sociedade Brasileira para o Estudo da Dor – SBED), the Brazilian branch of the International Association for the Study of Pain. The SBED was created by initiative of Pagura and the neurologist Moacir Schnapp. Pagura was elected the second president of this society. Jose´ Oswaldo Oliveira Jr (> Figure 16-9a) graduated from the USP Medical School in 1977, institution where he also did his residence training from 1978 to 1982. In 1984 he obtained his master degree, and in 1986, his PhD, both from the USP Medical School. His training in functional neurosurgery was done in Edinburgh,

under the supervision of Edward Hitchcock, in 1985 (7 months), and in Paris, supervised by Gabor Szikla, in 1986 (9 months). A very inventive person, in the 1980s, time in which the radiofrequency generators (RFG) in Brazil had to be imported, with technical assistance, he built his own equipment, not for commercial purposes, but for his personal use. Two other versions of this RFG were later developed. The main drawback of his equipment was the lack of temperature monitoring, which had to be inferred based on the amperage. Placement of the DBS electrode is, to say the least, a quite boring and time consuming maneuver, as everyone involved with this technique knows. In 2005, Oliveira Jr developed the DBS electrode placer (> Figure 16-9b), later commercialized by Micromar. This very simple equipment makes DBS electrode placement an easy and fast procedure. Besides, he also developed a head and electrode holder for percutaneous cordotomy, a kit for transsphenoidal chemical hypophysectomy, and a number of electrode kits. Oliveira Jr heads the Department of Functional Neurosurgery, Antalgic Therapy and Palliative Care at AC Camargo Hospital, the most important and antique institution for cancer treatment in Brazil, and the Functional Neurosurgery Service at the Division of Neurosurgery at Servidores Pu´blicos Estaduais Hospital, both in Sa˜o Paulo. Although also a very versatile functional neurosurgeon, his main area of interest and expertise has always been pain surgery. During his very active career, he has formed more than 20 functional neurosurgeons. Cla´udio Fernandes Correˆa (> Figure 16-10) graduated from the Federal University of Triaˆngulo Mineiro in 1978 and did his neurosurgical residence (1979/1982) at Beneficeˆncia Portuguesa Hospital, in Santos, Sa˜o Paulo State. Correˆa obtained both his master degree (spinal cord stimulation for refractory pain, 1994) and PhD (brachytherapy for brain tumors, 1999) at the Paulista Medical School, Federal University

History of stereotactic and functional neurosurgery in brazil

16

. Figure 16-9 (a) Jose´ Oswaldo Oliveira Jr (b) Micromar electrode placer

. Figure 16-10 Cla´udio Correˆa

of Sa˜o Paulo. His formation in stereotactic and functional neurosurgery was initially supervised by Carlos Telles (1986/1987), and later by Manoel Teixeira. At present he heads the Stereotactic and Functional Neurosurgery Service at Nove de Julho Hospital, in Sa˜o Paulo. His main areas of expertise are pain surgery and stereotactic neurooncology. So far Correˆa has performed more than 1,300 microcompressions of the gasserian ganglion [62], which probably represents one of the largest series in the world. His experience in brachytherapy is also impressive [52], seconding only that of

Teixeira in our country. Correˆa was president of the Brazilian Society for Stereotactic and Functional Neurosurgery in the biennium 1996/1998 and the founder of SIMBIDOR, a biennial multidisciplinary pain meeting, with already eight versions (first version: 1994), undoubtedly one of the most important Brazilian pain meetings. Arthur Cukiert graduated from the USP Medical School in 1986, completing his neurosurgical training at the same institution in 1990 (1987/1990). He then moved to Montreal Neurological Institute, where he trained in epilepsy and stereotactic surgery with Andre Olivier (1991/1992). Since he returned to Brazil Cukiert has headed the Division of Neurology and Neurosurgery at Brigadeiro Hospital, in Sa˜o Paulo. In 1996, he obtained his PhD at the USP. Almost all his practice has been dedicated to epilepsy and pituitary tumor surgery. So far he has performed more than 1,200 epilepsy surgeries. Cukiert has published extensively on all aspects of epilepsy [63–68]. His main interests in this area are the normal and abnormal function of the corpus callosum and the development of clinical and flowchart paradigms for the medical and surgical treatment of epilepsy. He is one of the authors of the first epidemiological paper on

215

216

16

History of stereotactic and functional neurosurgery in brazil

epilepsy released in Brazil [63]. Cukiert was also the first in the country to perform deep brain stimulation for the treatment of refractory epilepsy (anterior thalamic nucleus). He is author of five books: three on epilepsy and two on neuroendocrinology. Jack Beraha graduated from the Pontifical Catholic University of Sa˜o Paulo Medical School in 1978. He did his neurosurgical training at Oswaldo Cruz Hospital (Sa˜o Paulo), supervised by Darcy Vellutini, going later to Geneva, where he accompanied the services of A. Werner and J. Berney. He then moved on to the University of Genebra, where he obtained his PhD. As he became interested in radiosurgery he went to the University of Valencia Medical School, staying with Barcia-Salorio in 1982/1983, and afterwards to Buenos Aires and Charlottesville, accompanying Ladislau Steiner for a period of 21=2 months. In 1987, Beraha became Full Professor at the Pontifical Catholic University of Sa˜o Paulo Medical School. Until 1983 radiosurgery was performed by using gamma-knife, telecobaltotherapy, proton beam, and betatron. During his stay with Barcia-Salorio, he learned about telecobaltotherapy radiosurgery. Using a principle similar to that of Barcia-Salorio, Beraha, helped by the physicists Luiz Scaff and Dirceu Vizeu, modified a 4 MeV linear accelerator (LINAC) at Oswaldo Cruz Hospital, in Sa˜o Paulo, to make it radiosurgery-compatible, and in July of 1983 Beraha et al performed the first LINAC radiosurgery in the world in a patient harboring a craniopharyngioma [69]. From then until 1989 he treated more than 100 patients presenting with intracranial tumors or arteriovenous malformations [69,70]. One of these patients, who had a vestibular schwannoma that apparently failed to respond to radiosurgery, was subsequently operated on by a very skillful and famous neurosurgeon. After the operation, this patient presented significant complications, and the neurosurgeon, seemingly in an attempt to get rid of the possible

implications of the poor result, told the patient’s family that the sequel was consequence of the prior radiosurgery. Beraha was sued by the patient’s family, but even having been proved innocent, as expected, the number of referrals declined drastically, and his radiosurgery service was finally closed in 1989. It must be remembered, however, that the world owes Jack Beraha the clinical introduction of LINAC radiosurgery. Also worth mentioning is the fact that this story was told us not by Beraha, but by a number of other colleagues. Nilton Luis Latuf (1937–2005) graduated from the USP Ribeira˜o Preto Medical School in 1963, where he also attended his residence in neurosurgery (1964/1966). In 1967 Latuf went to Paris and spent 1 year with Gerard Guiot at Foch Hospital [71]. Back to Brazil and to Ribeira˜o Preto, in Sa˜o Paulo State, he was the first functional neurosurgeon in Brazil to establish his practice in the countryside. His first functional procedure, a thalamotomy in a parkinsonian patient, was performed by using the Guiot frame, and it took place at Santa Casa de Miserico´rdia Hospital, in Ribeira˜o Preto, in October 1968. In 1969 Latuf inaugurated the Division of Neurology and Neurosurgery in the same institution, heading it for 25 years. He formed 48 residents, and performed more than eight thousand neurological surgeries throughout his life [71], a significant amount of these constituted by stereotactic and functional neurosurgery procedures. Latuf was a member of the executive council of the Brazilian Society of Neurosurgery for 21 years, as well as the South American Representative and Honorary President of the World Association of Lebanese Neurosurgeons for many years. A number of other colleagues in Sa˜o Paulo State have established a busy practice in the field of stereotactic and functional neurosurgery, among them: Erich Fonoff (Sa˜o Paulo), Nilton Lara (Sa˜o Paulo), Salomon Benabou (Sa˜o Paulo), Valter Cescato (Sa˜o Paulo), Antoˆnio de Almeida

History of stereotactic and functional neurosurgery in brazil

(Sa˜o Paulo), Evandro de Souza (Sa˜o Paulo), Soraya Cecı´lio (Sa˜o Paulo), Jose´ Cla´udio Marinho da No´brega (Sa˜o Paulo), Luis Augusto Rogano (Sa˜o Paulo), Edson Amaˆncio (Santos), Arthur Ungaretti Jr (Santo Andre´), Joa˜o Alberto Assirati Jr (Ribeira˜o Preto), Marcus Colbachini (Ribeira˜o Preto), Sebastia˜o Carlos da Silva Jr (Sa˜o Jose´ do Rio Preto), Kleber Duarte (Sa˜o Jose´ do Rio Preto), Carlos Tadeu Parisi Oliveira (Braganc¸a Paulista), Guilherme Cantatore Castro (Braganc¸a Paulista), Jose´ Paulo Montemor (Campinas), and Edmur Piza Filho (Jundiaı´).

Minas Gerais State The pioneer of stereotactic and functional neurosurgery in Minas Gerais State was Jose´ de Arau´jo Barros. Jose´ de Arau´jo Barros (> Figure 16-11a) graduated from the Federal University of Minas Gerais Medical School and in 1953 he finished his initial training in neurosurgery with Francisco Rocha, a disciple of Herbert Olivecrona and one of the pioneers of neurosurgery in Minas Gerais State. In 1954 he moved on to the University of Illinois in Chicago, spending 2 years under Percival Bailey. During his fellowship, he went several times to New York to learn stereotactic surgery with Irving Cooper. Back to Belo Horizonte, capital of Minas Gerais State, Barros constructed his own frame (> Figure 16-11b), based on that of Cooper, and started performing stereotactic surgery in 1960. This was the first stereotactic apparatus built in Brazil. Along the years he performed 248 procedures in 186 patients harboring movement disorders, mainly Parkinson’s disease, but also dystonia, hemiballism, and choreoathetosis. In 1961 he became Full Professor of Neurology at the Minas Gerais Medical Sciences School, position that he occupied until his retirement in 1998. A very active neurosurgeon at Sa˜o Jose´ Hospital, the teaching hospital of the Medical

16

Sciences School, Barros formed 58 neurosurgeons. One of his ex-residents, Lourenc¸o de Freitas Neto, replicated his frame and was the pioneer in the stereotactic field in Espı´rito Santo State. At present, five are the best known and active functional neurosurgeons in Minas Gerais: Jose´ Maurı´cio Siqueira, Gerva´sio Teles Cardoso de Carvalho, Sebastia˜o Nataniel Silva Gusma˜o, Rodrigo de Mattos Labruna, and Gilberto de Almeida Fonseca Filho. Jose´ Maurı´cio Siqueira graduated from the Federal University of Minas Gerais Medical School in 1976 and attended neurosurgical residence at Felı´cio Roxo Hospital (1977/1979), in Belo Horizonte, previously one of the two teaching hospitals at the Federal University of Minas Gerais. In 1981 he went to the University of Toronto, spending 1 year as a fellow under Ronald Tasker. Consecutively, he accompanied Claude Bertrand at the Notre Dame Hospital for 2 months and Patrick Kelly, at the New York State University at Buffalo, for 1 month. Some years later he also spent a short period (1 month) with Erik Backlund at the Karolinska Institute in Stockholm. Siqueira made two major contributions to the field of stereotactic and functional neurosurgery. In 1985 Siqueira was the first in the literature to describe the technique of open bulbospinal trigeminal nucleotomy through radiofrequency lesioning for the treatment of refractory facial deafferentation pain [72]. This paper, in which he reported the 1-year follow-up results obtained in two patients operated on in 1983 (complete abolition of pain was achieved in both patients), had been previously presented as a poster at the IX Meeting of the World Society for Stereotactic and Functional Neurosurgery in Toronto, in 1985, chaired by Ronald Tasker. In 1986, Blaine Nashold et al published an abstract in Neurosurgery describing a technique identical to that of Siqueira, claiming that this ‘‘new surgery’’ had

217

218

16

History of stereotactic and functional neurosurgery in brazil

. Figure 16-11 (a) Jose´ de Arau´jo Barros (b) Stereotactic frame built by Barros

been developed by his group [73]. Actually, Nashold has never mentioned Siqueira’s pioneer paper in any of his publications. In 1987, in a letter sent to the editor of Neurosurgery, Schvarcz contested the idea that Nashold was the original author of the technique and stated that Hitchcock and himself, in 1972, were the first to report that technique, using the stereotactic approach, and mentioned Siqueira’s poster, who had performed the procedure through an open operation [74]. Schvarcz, however, failed to mention that the very first to perform this procedure by employing the stereotactic technique was Edward Hitchcock alone in 1970 [40]. In 1997, during the 11th Congress of the World Federation of Neurosurgical Societies, held in Amsterdam, Tasker introduced Siqueira to John Gorecki, an ex-resident of Nashold’s, and told him about the pioneer paper of Siqueira. Afterwards, Siqueira sent Gorecki a reprint of his paper, as well as the certificate of his poster presentation of 1985 at the World Society for Stereotactic and Functional Neurosurgery Meeting in Toronto. In 2004 Gorecki, in his chapter on DREZ and brainstem ablative procedures for Youmans Neurological Surgery fifth edition, finally gave Siqueira the deserved credit, reputing his report in this issue as the first published in the literature [75].

During his fellowship at the University of Toronto, Siqueira helped to review Tasker’s experience on unilateral Vim thalamotomy for the treatment of severe drug-resistant parkinsonian tremor. The conclusions derived from this study, published in 1983, when very few was being said about the surgical treatment of Parkinson’s disease, were very instrumental for the renascence of interest in this modality of treatment [76]. Currently, Siqueira heads the Services of Functional and Epilepsy Surgery of the Division of Neurology and Neurosurgery at Felı´cio Roxo Hospital. Gerva´sio Teles Cardoso de Carvalho graduated from the Minas Gerais Medical Sciences School in 1981. He finished his residence training at Santa Casa de Miserico´rdia de Belo Horizonte Hospital in 1985 (1982/1985), and spent 1 year (1986) with Carlos Telles at Pedro Ernesto Hospital, the teaching hospital at the State University of Rio de Janeiro. In 1987, following the lead of Siqueira, he went to the University of Toronto and spent 1 year under Ronald Tasker (1987/ 1988). In 1995 he obtained his master degree from the Federal University of Sa˜o Paulo. Carvalho has a vast experience in the surgical treatment of pain [77–79], psychiatric and movement disorders [80], and coordinates the

History of stereotactic and functional neurosurgery in brazil

Stereotactic and Functional Neurosurgery Service at the Division of Neurosurgery at Santa Casa de Miserico´rdia de Belo Horizonte Hospital. During the time he was a fellow under Tasker, he was part of the team that demonstrated that, in patients suffering from cord injury pain, the intermittent neuralgic and evoked elements of neuropathic pain differed from the steady causalgic/dysesthetic element in their response to destructive and modulatory procedures (the latter, contrarily to the first two elements, which are frequently relieved by interruption of the pain pathways, responds better to stimulation of the spinal cord or the brain), suggesting the presence of distinct mechanisms underlying these different modalities of pain [77–79]. Sebastia˜o Nataniel Silva Gusma˜o graduated from the Minas Gerais Medical Sciences School in 1973 and did his neurosurgical residence in the same institution (1974/1976). Three years later, to polish his initial formation, he spent 1 year at the Department of Neurosurgery at the National Hospital for Nervous Diseases, in London, and a shorter period at the Louis Pasteur University Medical School, in Strasbourg. Gusma˜o obtained his master degree from the Federal University of Minas Gerais in 1984, and his PhD from the Federal University of Sa˜o Paulo in 1993. His training in stereotactic and functional neurosurgery was done under Carlos Telles, in Rio de Janeiro, and also, for a shorter period, at Stockholm University. Gusma˜o was president of the Brazilian Society for Stereotactic and Functional Neurosurgery in the biennium 1992/1994 and is currently Full Professor of Neurosurgery and Head of the Division of Neurosurgery at the Federal University of Minas Gerais. Pain surgery constitutes his main area of expertise in the field of stereotactic and functional neurosurgery, and from this area derived his most important contribution. Gusma˜o was the first in the literature to propose the use of intraoperative computed tomography to guide percutaneous

16

radiofrequency trigeminal rhizotomy, greatly facilitating the identification of the foramen ovale [81]. Two other very experienced colleagues from Minas Gerais are Rodrigo de Mattos Labruna, trained by Teixeira, and Gilberto de Almeida Fonseca Filho, trained by Teixeira, Dieckmann and Ostertag. Their main areas of expertise are pain and spasticity surgery. Labruna has also a significant experience in surgery for psychiatric disorders.

Espı´rito do Santo State The pioneer of stereotactic and functional neurosurgery in Espı´rito Santo State was Lourenc¸o de Freitas Neto. Freitas Neto did his residence training in Belo Horizonte under Jose´ de Arau´jo Barros, who introduced him to stereotactic surgery. He then moved back to Vito´ria, the capital of Espı´rito Santo, in 1968, where, after replicating the frame developed by Barros, he started performing stereotactic surgery for movement disorders. Until 1984 he performed 32 procedures, basically for Parkinson’s disease, occasion in which he abandoned functional neurosurgery due to the lack of candidates for surgery. Se´rgio Otoni, after a 6-month training with Edward Hitchcock, returned to Vito´ria in 1978, but never really dedicated to stereotactic and functional neurosurgery. Pedro Menezes, trained by Teixeira, worked part of the time in Sa˜o Paulo and part in Vito´ria. Between 2000 and 2006, while in Vito´ria, he performed a significant number of functional procedures. Only recently (2003), though, Walter Fagundes-Pereyra for the first time established a really active and ongoing practice in functional neurosurgery in Espı´rito Santo (Vito´ria). Fagundes-Pereyra was first exposed to stereotactic and functional neurosurgery by Gerva´sio Carvalho, during his neurosurgical residence at Santa Casa de Miserico´rdia de Belo Horizonte Hospital. In 2001 he obtained his master degree from the same institution. He

219

220

16

History of stereotactic and functional neurosurgery in brazil

then moved on to Lille, where, during 1 year and a half, he refined his training in stereotactic and functional neurosurgery with Serge Blond. In 2007 he obtained his PhD from the Federal University of Sa˜o Paulo.

Midwest Region The Midwest region is composed by the states of Goia´s, Mato Grosso, and Mato Grosso do Sul and the Federal District.

Goia´s State The pioneer of stereotactic and functional neurosurgery in the Midwest region was Luiz Fernando Martins (> Figure 16-12), undoubtedly one of the most renowned and important functional neurosurgeons in Brazil and South America. Martins graduated from the Federal University of Goia´s Medical School in 1971. His internship

. Figure 16-12 Luiz Fernando Martins

(1971), the last year (sixth) of Medical School in the Brazilian university system, was spent with Renato Barbosa, at Lagoa Hospital, in Rio de Janeiro. Barbosa was the one who first introduced him to stereotaxis. Since then, and certainly forever, Martins became a victim of a platonic love for this marvelous field of neurosurgery. In 1972 he went to the University of Berlin, where he stayed for a period of 4 years, doing his neurosurgical residence under Wilhelm Umbach, at the time one of the most important functional neurosurgeons in Germany. In 1975 Martins obtained his PhD from the University of Berlin, and in 1976, back to Brazil, he started his practice in Goiaˆnia, the capital of Goia´s, joining the team of the Goiaˆnia Neurological Institute, a private hospital founded the year before, then and now one of the most important neurosurgical institutions in the country. On 13 February 1976, using a Riechert and Mundinger apparatus, he performed his first stereotactic procedure, lesioning the zona incerta in a patient presenting with Parkinson’s disease. In 1982 he returned to Europe, spending more than 1 year: 3 months with Brock, in Berlin; 2 months with Dieckmann, in Go¨ttingen; 7 months with Siegfried, in Zurich; and 2 months with Mundinger, in Freiburg. A team player, Martins has always proclaimed the need of a multidisciplinary group to evaluate surgical candidates in all areas of functional neurosurgery. Though performed in an irregular basis since 1976, only in 1989 the epilepsy surgery program was inaugurated at Goiaˆnia Neurological Institute. Thanks to this government-supported program, for which implementation were instrumental Martins, the neurosurgeon Orlando Arruda, and the epileptologist Paulo Ragazzo (trained at the Montreal Neurological Institute), 1,782 patients, not only from the Midwest, but also from the North and Northeast of the country could be operated on in this institution. These operations should be credited to the following team of neurosurgeons: Luiz Fernando Martins, Orlando Arruda (already

History of stereotactic and functional neurosurgery in brazil

dead), Valter da Costa, Joa˜o Arruda, Joaquim da Costa, and more recently, Henrique Lobo, Marcelo Martins, and Osvaldo Vilela Filho. In 1999 Martins innovated again, creating the first radiosurgery service in the Midwest region, and one of the first in the country. This service is a joint project of Goiaˆnia Neurological Institute and CEBROM (Brazilian Center of Radiotherapy, Oncology and Mastology), a private outpatient clinic dedicated to oncology, radiotherapy and chemotherapy and owner of the LINAC used in the procedures. Since then, three hundred and 16 radiosurgeries have been performed. Both epilepsy surgery and radiosurgery programs are clear examples of a multidisciplinary team work. Martins is a highly experienced neurosurgeon in all areas of stereotactic and functional neurosurgery, but spasticity. Throughout his outstanding career he has performed, besides those aforementioned, 402 surgeries for movement disorders (mainly Parkinson’s disease); 714 for pain (mainly trigeminal neuralgia); 468 for psychiatric disorders (mainly aggressiveness and OCD), probably one of the largest series in the world at present; 186 stereotactic biopsies; and 36 stereotactic-guided craniotomies. Martins was one of the founders of the Brazilian Society for Stereotactic and Functional Neurosurgery, being its president for two terms (1984/1986 and 2000/2002), and of the recently created Brazilian Society of Radiosurgery (2007), which has as president the functional neurosurgeon Salomon Benabou, and is now president of the SLANFE (Latin American Society for Stereotactic and Functional Neurosurgery). Though author of just a few papers [82–88], he made two significant scientific contributions: the determination of the radiographic stereotactic coordinates of the foramen ovale [82], and the correlation between the position and size of medial thalamic lesions and the degree of pain relief obtained by patients presenting cancer pain (an autopsy study) [83,84]. Another important contribution, although not published, was his

16

proposal of combined amygdalotomy and anterior capsulotomy for the treatment of refractory aggressiveness (1985). But as he says, ‘‘I am not a writer, but a surgeon. I like to operate and also to lecture, this is how I have chosen to pass along my experience.’’ A superb lecturer, he played a very important role spreading the knowledge concerning surgical treatment of psychiatric disorders, movement disorders, and epilepsy across the country. Unfortunately, the lack of habit of writing papers is a characteristic shared by the vast majority of Brazilian neurosurgeons, which seems to be a cultural deficiency. How much more could someone like him have contributed to the field by writing down such a huge experience. There are six other functional neurosurgeons in Goia´s State, five of them from Goiaˆnia and one from Ana´polis (Nivaldo Evangelista Teles). Four of those from Goiaˆnia are part of the team of the Goiaˆnia Neurological Institute (Joaquim da Costa, Joa˜o Batista Arruda, Vladimir Arruda Zaccariotti, and Osvaldo Vilela Filho), and the other one has his Service at Santa Helena Hospital (Hamilton Ayres da Silva). Hamilton da Silva, once finished his 5-year residence in neurosurgery (1987/1991) at Servidores Pu´blicos Estaduais Hospital (Sa˜o Paulo), decided to dedicate his career to stereotactic and functional neurosurgery and spent 4 years (1992/ 1995) with Teixeira at USP Medical School and 6 months (1996) with Ronald Tasker at University of Toronto. Eventually he returned to Goiaˆnia and established his practice at Santa Helena Hospital and Goiaˆnia General Hospital. Most of his practice in stereotactic and functional neurosurgery has been devoted to the surgical treatment of pain. Joaquim da Costa had his initial contact with stereotaxis as a resident under Jose´ de Arau´jo Barros, the pioneer of stereotactic and functional neurosurgery in Minas Gerais State, but his true master was Martins, with whom he works until now. In 1983 he spent a short period with Falk Oppel in Berlin learning epilepsy surgery.

221

222

16

History of stereotactic and functional neurosurgery in brazil

Like Martins, he is a very experienced functional neurosurgeon. Joa˜o Arruda and Vladimir Zaccariotti did their neurosurgical residence at Goiaˆnia Neurological Institute. Both had Martins as their first master in stereotactic and functional neurosurgery. Arruda completed his training with Blaine Nashold at Duke University (1 year), and Zaccariotti, with Falk Oppel (17 months), in Bielefeld, and Antonio De Salles, at UCLA (7 months). Arruda works both at Goiaˆnia Neurological Institute and Arau´jo Jorge Hospital (Cancer Hospital), where he runs the Neurosurgical Service, devoted mainly to neurooncology, treatment of pain and radiosurgery, areas in which he has a large experience. Besides, he is also a very experienced epilepsy surgeon. Zaccariotti works with him in both institutions. Osvaldo Vilela Filho (> Figure 16-13) graduated from the Federal University of Goia´s (Universidade Federal de Goia´s – UFG) Medical School in 1984. During his last 2 years of Medical School, he accompanied many functional procedures performed by Luiz Fernando Martins at Goiaˆnia Neurological Institute, one of his . Figure 16-13 Osvaldo Vilela Filho

personal icons. This simple fact would later influence his whole career. His neurosurgical residence (1985/1988) was done at the Brası´lia District Hospital, in Brası´lia, being chief resident of neurosurgery in 1988. Unfortunately, stereotactic and functional neurosurgery was not performed in this institution at that time. Worried about the difficulty to approach some lesions of difficult location, mainly those deeply placed, Vilela Filho (1987) developed a technique that allowed the transposition of the lesions seen on CT-scan to the scalp, greatly easing the surgical procedure [89]. Later, before his stereotactic training, he used the same technique to perform CT- or ultrasound-guided free-hand biopsy of intracranial lesions [90]. In February of 1991 he went to the Toronto Western Hospital, University of Toronto, to do a fellowship in stereotactic and functional neurosurgery under Ronald Tasker, staying until 1992. While at UT he reviewed all patients with neuropathic pain submitted to DBS by Ronald Tasker. This research led to a number of important publications [91–95]. Tasker became another of his icons, with whom he established a close friendship that remains until now, someone that he gladly reputes as his Canadian father. In 1993 he returned to Canada, this time to the University of Western Ontario, in London, to learn epilepsy surgery under the supervision of Andrew Parrent and John Girvin. Later he went to other centers of excellence in stereotactic and functional neurosurgery for shortperiod visits, like those of Roy Bakay, at the time at Emory University (2000); Andres Lozano, at University of Toronto (2000); and Ali Rezai, at Cleveland Clinic (2004). In 2006 he obtained his PhD from the Paulista Medical School, Federal University of Sa˜o Paulo. Back to his hometown, Vilela Filho inaugurated and headed the Goiaˆnia Brain Institute, devoted to neurosurgery and neurology, in general, but particularly to stereotactic and functional neurosurgery. Initially located at the Goiaˆnia Orthopedic Institute (1993/2001), it

History of stereotactic and functional neurosurgery in brazil

was later moved to Lucio Rebelo Hospital (2001/ 2003). In 1994 he underwent a competitive examination for neurosurgeon of the UFG Medical School, achieving the highest score, and since 1995 he has worked as an Invited Professor of Neurosurgery in the Department of Surgery of the same institution. After 3 years of continuous insistence, the Clinic Hospital, teaching hospital of the UFG Medical School, finally acquired the necessary equipment and in 1998 he created the Stereotactic and Functional Neurosurgery Service at the Division of Neurosurgery at the Clinic Hospital, which he has chaired since then. This was the first university and public hospital in the Midwest region of the country to offer stereotactic and functional neurosurgery. In 2001 Vilela Filho inaugurated the Laboratory of Experimental Stereotaxis at the UFG Medical School, which he still runs. In 2002 he became a consultant in neurosurgery and neurology to the Council of Healthcare Advisors, which was presided by the Nobel Laureate James Watson (dead in 2004), and in 2003 he became part of the team at the Goiaˆnia Neurological Institute. Since 2006 he has worked as an Invited Professor of the Department of Medicine at the Catholic University of Goia´s, becoming Associate Professor of Neurosciences after a competitive examination in 2007, once more achieving the highest score. Vilela Filho has had a very intense associative activity. Still as a student, he became a member of the Society for the Defense of Natural Resources (1977), a society made up almost exclusively by professors and researchers of the local universities (Federal and Catholic Universities of Goia´s), serving as its first secretary (1980/1982) and president (1982/1984). In 1997 he founded the Young Neurosurgeons Committee of the Brazilian Society of Neurosurgery, becoming its coordinator for three consecutive terms (1997/2002), and in the same year he was the chairman of the Scientific Committee of the VII National Congress of the Brazilian Academy of Neurosurgery. Again in 1997 he was one of the

16

founders and the first president of the Goia´s Association for the Study of Pain, position that he held for three terms (1997/2002), period in which he presided two important international congresses on pain, the I and II INDOR (International Congress on Pain). In 1999 he was also one of the founders and the first president of the Goia´s Society of Neurosurgery (1999/2002), presiding in 2001 its first congress, the first joint meeting Brazil & Canada on neurosurgery. For two consecutive terms he served as member of the International Relations Committee of the Brazilian Society of Neurosurgery (2000/2004), and in 2002 he was elected member of the Executive Council of this society (2002/2008). In 2004 he chaired the Scientific Committee of the XXV Brazilian Congress of Neurosurgery, organized by the Brazilian Society of Neurosurgery. Vilela Filho has been a true soldier of the Brazilian Society for Stereotactic and Functional Neurosurgery, having served as its secretary (2000/2002), vice-president (2004/2006), and president (2006/2008). In 2007 he presided the Eighth Congress of the Brazilian Society for Stereotactic and Functional Neurosurgery & First International Joint Meeting on Stereotactic and Functional Neurosurgery, undoubtedly the most important meeting organized by the Brazilian society. During this event was founded the Brazilian Neuromodulation Society, the Brazilian branch of the International Neuromodulation Society, and Vilela Filho was elected its vicepresident. In 2008 he became secretary of the Latin American Society for Stereotactic and Functional Neurosurgery (SLANFE). He is also member of a number of other societies, including the World and American Societies for Stereotactic and Functional Neurosurgery, International Neuromodulation Society, Brazilian Society for the Study of Pain, and American Association of Neurological Surgeons (1995/2002). Vilela Filho is member of the editorial board of three international journals (Neuromodulation; Brazilian Contemporary Neurosurgery, the

223

224

16

History of stereotactic and functional neurosurgery in brazil

Brazilian supplement of Surgical Neurology; and Neurotarget, the official journal of the Latin American Society for Stereotactic and Functional Neurosurgery) and six Brazilian journals (Neurocirurgia Contemporaˆnea Brasileira; Jornal Brasileiro de Neurocirurgia; Dor – 2002/2004; Simbidor; Jovem Me´dico; and Pra´tica Hospitalar), and was Associate Editor of the SBN Newsletter, the bulletin of the Brazilian Society of Neurosurgery (2002/2004). Throughout his career, Vilela Filho and his team have made numerous original scientific contributions, besides those aforementioned. Reviewing Tasker’s 16 patients with neuropathic pain of spinal cord origin submitted to DBS (thalamic ventrocaudal nucleus – VC and periventricular gray matter – PVG), he identified four patients with complete cord injury. PVGDBS was performed in three of these patients to treat the evoked and intermittent components of their pain, being unsuccessful in all them. VC-DBS, however, was successful in three out of four patients. Based on these results he contested previously proposed hypotheses, according which VC-DBS produces pain relief by inhibition of dorsal horn nociceptive neurons through a variety of pathways, which could not be at work in patients presenting complete cord transection [96,97]. Alternatively, he proposed that VC-DBS induces pain relief by inhibition of medial thalamus nociceptive neurons through a polysynaptic pathway, as follows: VC stimulation » somatosensory cortex excitation (» motor cortex activation) » anterior putamen excitation » peptidergic (substance P) activation of GPi/ SNR » medial thalamus inhibition [97]. Vilela Filho later proposed that this polysynaptic pathway would be operative even under physiological circumstances and could work as a modulatory pain center, which led him to name it as prosencephalo-mesencephalic modulatory circuit [98,99]. He also suggested that the interruption of this circuit or of its activating pathway, which he supposed to be the anterior spinothalamic

tract, by determining overactivation of the medial pain system, would be the pathophysiological substrate of the steady dysesthetic component of neuropathic pain [98,99]. According to his hypothesis, stimulation of various structures such as the peripheral nerves, spinal cord, medial lemniscus, VC, internal capsule and motor cortex induces pain relief by activation of this circuit [100,101]. Still in the field of pain surgery, Vilela Filho introduced the CT-guided percutaneous technique to perform punctuate midline myelotomy [102]; proposed the use of doppler-scan for localization of the occipital artery, which lies just lateral to the greater occipital nerve, greatly facilitating the realization of percutaneous radiofrequency occipital neurotomy and occipital nerve stimulation [103]; and was the first to propose the use of MRI for postoperative evaluation of percutaneous cordotomy [104]. It is well known that functional neuroimaging studies may frequently show abnormalities in patients harboring psychiatric disorders and that these abnormalities tend to disappear after successful surgical treatment. Vilela Filho, however, was the first to propose the use of functional studies to determine the best target to treat each patient. The idea was to surgically deactivate the areas shown to be hyperactive in the functional studies [105]. Some other studies performed by other authors, based on the principle suggested by Vilela Filho, led to the discovery of Brodmann area 25 as a target for depression [106] and of the posteromedial hypothalamus as a target for cluster headache [107]. Vilela Filho and Souza, in 1996 [108], and again in 1998 [109], originally proposed that Tourette syndrome is the clinical manifestation of the hyperactivity of the globus pallidus externus and prefrontal area. Based on this hypothesis, Vilela Filho et al, in 2004, were the first to perform bilateral GPe-DBS for the treatment of Tourette syndrome refractory to conservative management [110]. Four patients have been operated on so far. The excellent results obtained

History of stereotactic and functional neurosurgery in brazil

lend support to the presented hypothesis [111– 113]. In 2001, Vilela Filho proposed a modification in the technique of stereotactic subcaudate tractotomy, using landmarks seen on CT-scan instead of those seen in the skull X-ray, as it was usually performed [114]. Vilela Filho and Silva current series of 54 patients harboring Parkinson’s disease submitted to unilateral subthalamotomy is one of the largest in the literature. They have shown that STN lesioning is a highly effective and safe procedure [115–117]. A possible complication of this procedure is hemiballism, which occurred in 11% of the patients. These authors demonstrated that damage to the dorsolateral territory of STN and concomitant sparing of the zona incerta seem to be essential for the development of hemiballism, and that the presence of intraoperative stimulation-induced dyskinesia and, possibly, levodopainduced dyskinesia apparently are significant risk factors for the development of this complication [117,118]. In 2001 Vilela Filho et al reported the case of a patient with unilateral essential tremor whose tremor completely disappeared after a stroke restricted to the contralateral posterior putamen, leading him to originally propose a role for the basal ganglia in the genesis of essential tremor, possibly through the hyperactivity of the posterior putamen [119]. To test this hypothesis, they used an animal model of essential tremor (harmaline-induced tremor) and showed that the harmaline-induced tremor could be greatly reduced by an electrolytic lesion placed in the ipsilateral posterior striatum of the rat, giving further support to the proposed hypothesis [120]. Vilela Filho et al., in 1997, introduced an apparently low-risk and accurate technique for CT-guided free-hand percutaneous biopsy of spinal cord tumors [121]. In 2001 Vilela Fiho and his colleagues developed a new product that did not increase the inherent MRI distortion and could be seen in the main MRI sequences used for stereotactic surgery (T1-weighted,

16

T2-weighted and inversion recovery). This product, however, was never patented or commercialized [122]. Vilela Filho and Carneiro Filho, in 2002, were the first to introduce the gamma probe in neurosurgery, which was initially used for intraoperative detection of brain tumors and to ascertain its complete removal [123]. In 2006 the same authors again pioneered using the gamma probe for intraoperative detection of epileptogenic areas during epilepsy surgery, a technique still in investigation that seems particularly helpful in non-mesial temporal lobe epilepsy [124]. Finally, Vilela Filho and Carneiro Jr developed an MRI-based frameless technique to determine the stereotactic coordinates. A very precise technique, it allows to perform sort of an image fusion (CT and MRI) without the necessity of any software other than those of the MRI and CT scanners [125].

Mato Grosso State The pioneer of stereotactic and functional neurosurgery in Mato Grosso State was Jony Soares Ramos. Ramos did his residence training at Lagoa Hospital, in Rio de Janeiro. The Head of the Neurosurgery Service, Ney Monteiro, who supervised his residence, was one of the disciples of Renato Barbosa, the pioneer of stereotactic and functional neurosurgery in Brazil. During the last year of his training (2001), he completed his formation in pain surgery accompanying Carlos Telles at Pedro Ernesto Hospital, the teaching hospital at the State University of Rio de Janeiro. In 2002 he started his practice in Cuiaba´, the capital of Mato Grosso, initially using an antique Riechert and Mundinger apparatus, which he had bought from Renato Barbosa, already retired for a long time, and later he acquired the Micromar stereotactic system. From the beginning to 2004, he worked with Bruno Silveira, who trained with Teixeira, but Silveira stopped functional neurosurgery in 2004, and Ramos carried on by

225

226

16

History of stereotactic and functional neurosurgery in brazil

himself. Already performing stereotactic procedures for movement disorders, pain and biopsy for some years, in 2007, oriented by Martins, Ramos performed his first operation for the treatment of a psychiatric disorder. He is still the only active functional neurosurgeon in the state.

Mato Grosso do Sul State Two general neurosurgeons have recently started performing stereotactic and functional neurosurgery in Campo Grande, capital of Mato Grosso do Sul State. Cesar Nicolatte did his residence in neurosurgery at the Beneficeˆncia Portuguesa Hospital (1996/2000), in Sa˜o Paulo, where he learned stereotactic and functional neurosurgery with Paulo Dorsa, arriving in Campo Grande in 2001. Joaquim Oliveira Vieira Jr did his neurosurgical training at USP Medical School (1995/ 1999), accompanying the functional procedures performed by Teixeira, Cescato, and Oliveira Jr. After his residency, he did his PhD at the Brigadeiro Hospital, in Sa˜o Paulo, oriented by Arthur Cukiert, and started his practice in Campo Grande in 2003. Nicolatte and Vieira Jr, working together, have recently started to perform stereotactic and functional neurosurgery procedures, so far restricted to percutaneous procedures for pain, stereotactic biopsy and stereotactic-guided craniotomy.

Federal District The Federal District, located in Goia´s State, houses Brası´lia, the capital of the country. It seems unbelievable that stereotactic and functional neurosurgery was inaugurated in Brası´lia only in the 1990s, but there are some explanations for that. First, Brası´lia is a very young city, having been founded only in 1960, when it became the country’s capital (until then Rio de Janeiro was the Brazilian capital). Second, Paulo Mello, the

pioneer of neurosurgery in Brası´lia (1961), went to England a few years after its inauguration. Mello spent 4 years (1964/1967) at the Newcastle Upon Tyne Hospitals, becoming acquainted with stereotactic surgery by the hands of John Hankinson. Returning to Brası´lia, he was appointed Head of the Division of Neurosurgery at Brası´lia District Hospital (1971). In 1973 he went to Freiburg and spent 1 month with Mundinger. Still in the seventies the hospital acquired a Riechert and Mundinger apparatus and a radiofrequency generator, but at the time few stereotactic operations were being performed everywhere and Mello, already involved with vascular neurosurgery, felt his interest in stereotactic and functional neurosurgery almost completely vanish. Besides, the surgical room equipped with the system for orthogonal teleradiography has never been built. Third, Carlos Telles, who did his neurosurgical residence at Brası´lia District Hospital, was incited by Paulo Mello to dedicate himself to stereotactic and functional neurosurgery. Accepting the suggestion, he went to Germany to attend a fellowship in this field, where he spent almost 5 years. During his last year there (1980), Telles was visited by Pedro Sampaio, Professor of Neurosurgery and Head of the Division of Neurosurgery at Pedro Ernesto Hospital, the teaching hospital at Rio de Janeiro State University, who invited him to join his team. Telles accepted his invitation and established his practice in Rio de Janeiro in 1980. Brası´lia, then, remained without its so needed functional neurosurgeon. In 1994 the Division of Neurosurgery at ´ Brasılia District Hospital was headed by Carlos Silve´rio de Almeida, who had attended a fellowship in England. Almeida was strongly determined to unearth the old Riechert and Mundinger apparatus and put it at work, and so he did. Orienting his 4th year neurosurgical resident Luiz Cla´udio Modesto Pereira, they transposed the lesion seen on the CT-scan to the stereotactic skull radiography and finally performed the first stereotactic

History of stereotactic and functional neurosurgery in brazil

procedure in Brası´lia, the drainage of a deeply placed brain abscess. Luiz Cla´udio Modesto Pereira, excited with this first step, decided to dedicate to the field and became the pioneer in stereotactic and functional neurosurgery in the Federal District. In 1995 he visited the services of Christopher Ostertag, in Freiburg (2 months); Robert Goodman, in New York (1 month); and Manoel Teixeira, in Sa˜o Paulo (1 month). In 1996 he spent 1 month with Rees Cosgrove, in Boston, and 15 days with Ronald Tasker, in Toronto. From 1995 to 1998 his practice in stereotactic and functional neurosurgery was constituted by sporadic procedures and restricted to anesthetic blockades for pain, stereotactic biopsy, stereotactic-guided surgery and spinal cord stimulation. Even though, Pereira was apparently the first in Brazil to perform stereotactic fibrinolysis with rTPA to treat intracerebral hematomas (1995). In 1999 he finally went to Toronto, spending 1 year under Andres Lozano at the University of Toronto, and since his return to Brası´lia (2000) he has established a full and busy practice in stereotactic and functional neurosurgery [126,127]. The second and last functional neurosurgeon in the Federal District so far is Tiago Freitas, who, like Pereira, was a resident at the Brası´lia District Hospital (2002/2005). Graduated from the Federal University of Goia´s Medical School (2001), during his last year of neurosurgical training he intermittently accompanied Vilela Filho at Goiaˆnia Neurological Institute. In 2006 Freitas went to USP Medical School, accompanying Manoel Teixeira for 3 months, and then to the Cleveland Clinic for a 7-month fellowship under Ali Rezai. Still in the same year he started his practice in Brası´lia.

South Region The South region is made up by the states of Parana´, Rio Grande do Sul and Santa Catarina.

16

The pioneer of stereotactic and functional neurosurgery in the South was Renato de Muggiati, from Parana´.

Parana´ State Renato de Muggiati (1932–1996) (> Figure 16-14) graduated from the Federal University of Parana´ in 1955. During his last 2 years at Medical School, he had the opportunity to accompany the neurosurgeon Jose´ Portugal Pinto, nephew of Jose´ Ribe Portugal, who had recently arrived in Curitiba (state capital) after 6 years at Cleveland Clinic under Gardner, inaugurating neurosurgery in this state. As an assistant to Pinto, he helped him to perform a large number of prefrontal lobotomies at Adauto Botelho Hospital. Finished his graduation, he continued at that institution until 1959, occasion in which he went to Freiburg, spending 2 years under Riechert. A Riechert and Mundinger apparatus was the most important piece of his luggage on his trip back to Curitiba. In 1961 he performed the first stereotactic procedure in Parana´ State, a

. Figure 16-14 Renato de Muggiati

227

228

16

History of stereotactic and functional neurosurgery in brazil

thalamotomy in a parkinsonian patient [128]. At the beginning, he built his own electrodes using the spokes from bike wheels. Still in 1961 he was invited to create and head the Division of Neurosurgery at the Clinic Hospital, the teaching hospital of the Federal University of Parana´, in fact the first university neurosurgical service in Parana´. In 1962 he inaugurated the Neurosurgery Service at Santa Casa de Miserico´rdia de Curitiba Hospital, which later became one of the teaching hospitals of the Pontifical Catholic University of Parana´ [128]. Despite being a general neurosurgeon, stereotactic surgery always remained as one of the most important activities in his outstanding career, along which he performed 304 stereotactic procedures, mainly for Parkinson’s disease [129]. The oldest functional neurosurgeon in Parana´ today is Alceu Correia, who trained with Wolfhard Winkelmu¨ller at the University of Hannover for 5 years (1971/1975). Correia has a vast experience in the surgical treatment of pain and was president of the Brazilian Society for Stereotactic and Functional Neurosurgery in the biennium 1994/1996. At present there are eleven other colleagues in Parana´ performing functional neurosurgery. However, stereotactic and functional neurosurgery constitutes the main area of activity of only four of them: Alexandre Novicki Francisco, Murilo Sousa Meneses, Danel Benzecry de Almeida, and Helve´rcio Fernando Polsaque Alves. Alexandre Novicki Francisco graduated from the Federal University of Parana´ in 1992. After finishing his neurosurgical residence at Santa Casa de Miserico´rdia de Curitiba Hospital in 1996, he went to the USP Medical School, spending 6 months with Teixeira (1997). The next step was the University of Toronto, where he did a 1-year fellowship under Ronald Tasker and Andres Lozano (1997/1998). Since his return to Curitiba in 1998 he has coordinated the Stereotactic and Functional Service at the Division of Neurosurgery at Cajuru Hospital, a

teaching hospital at the Pontifical Catholic University of Parana´. His main areas of expertise are the surgical treatment of pain [95,130], spasticity and movement disorders. Francisco was secretary of the Brazilian Society for Stereotactic and Functional Neurosurgery (2006/2008), and is now vice-president (president-elect) of the same society and secretary of the Brazilian Neuromodulation Society, the Brazilian branch of the International Neuromodulation Society (INS). Murilo Sousa Meneses graduated from the Federal University of Parana´ in 1980. He then went to France for a 6-year residence in neurosurgery. During his last year (1987), at Lariboisiere Hospital (Paris) under Claude Thurel, Meneses got most of his training in stereotactic and functional neurosurgery. In 1987 he obtained his master degree, and in 1990 his PhD, both from the University of Picardie, in Amiens. In 1988, back to Curitiba, he became Assistant Professor of Anatomy (neuroanatomy) at the Federal University of Parana´; he is now Associate Professor of the same discipline. His initial formation in stereotactic and functional neurosurgery was later complemented with short-period (1 month) visits to other centers of excellence in the field, such as Mayo Clinic, with Patrick Kelly (1991); Saint Anne Hospital (Paris), with Chudkiewicz (1993); University of South California, with Michael Appuzzo (1994); and in Bordeaux, with Alain Rougier (1998). The areas in which he is most experienced are epilepsy [131–133] and movement disorders [134] surgery. Meneses is the author of three books, one in Parkinson’s disease (two editions), and two in neuroanatomy (one of them with two editions). Daniel Benzecry de Almeida graduated from the Federal University of Para´ in 1990. His neurosurgical residence was done at Paulista Medical School, Federal University of Sa˜o Paulo (1991/ 1994). In 1995 he started his training in stereotactic and functional neurosurgery, spending 1 year with Teixeira at USP Medical School (1995/1996), and after that, another year with

History of stereotactic and functional neurosurgery in brazil

Oliveira Jr at AC Camargo Hospital (1996/1997). In 1998 he went to Lyon for a 3-month fellowship under Marc Sindou. Later he visited Richard North at Johns Hopkins for a short period (2 weeks). Almeida dedicates most of his practice to pain surgery [135,136]. In 2007 he obtained his master degree from the Federal University of Sa˜o Paulo. Helve´rcio Fernando Polsaque Alves graduated from the State University of Maringa´ in 1997. Once finished his residency at Santa Casa de Miserico´rdia de Ribeira˜o Preto Hospital (2001), where he was first exposed to stereotactic surgery by Nilton Latuf and Marcus Colbachini, he spent 15 months at AC Camargo Hospital under Oliveira Jr. In 2003 he went to Maringa´, a beautiful and relatively small town in the interior of Parana´, where he established his busy practice in stereotactic and functional neurosurgery, consisting predominantly of surgical treatment of pain and movement disorders. The other colleagues performing stereotactic and functional neurosurgery in Parana´ to a lesser extent are: Ce´sar Vinicius Grande, Sonival Caˆndido Hunhevicz, Sı´lvio Machado, and Samir Ale Bark, in Curitiba; Stenio H. de Souza, in Cascavel; and Pedro Garcia Lopes and Wander Miguel Tamburus, in Londrina.

Rio Grande do Sul State The pioneer of stereotactic and functional neurosurgery in Rio Grande do Sul was Paris Ferreira Souza. Paris Ferreira Souza (> Figure 16-15) graduated from the Federal University of Rio Grande do Sul in 1952. His neurosurgical training was done at USP Medical School, under Rolando Tenuto, from 1954 to 1958. Willing to polish his neurosurgical technique, Souza went to Mainz, accompanying Schu¨rmann for 2 years (1961/1963). Before leaving Germany, he decided to go to Freiburg, where he spent 2 months with Riechert and Mundinger to learn stereotactic

16

. Figure 16-15 Paris Ferreira Souza

surgery and purchased a Riechert and Mundinger apparatus. Back to Brazil, he decided to return to Porto Alegre, capital of Rio Grande do Sul, and start his practice. Still in 1963 Souza performed his first stereotactic procedure to treat a patient with Parkinson’s disease at the Beneficeˆncia Portuguesa Hospital, in Porto Alegre, becoming the pioneer of stereotactic and functional neurosurgery in this state. Due to some problems of political nature, however, he had to leave Porto Alegre in 1964. In 1965 he restarted his stereotactic practice in Sa˜o Paulo, at Oswaldo Cruz Hospital, a private institution. A joint project of Oswaldo Cruz Hospital and Servidores Pu´blicos Estaduais Hospital, a public institution, allowed him to operate on patients of the public hospital in the private hospital. Until the beginning of the 1970s he operated on a lot of parkinsonian patients, occasion in which he abandoned functional neurosurgery due to the sharp decline in surgical indications and went on as a general neurosurgeon. Paris Souza is now 84 years old, the oldest Brazilian functional neurosurgeon alive. He spends his lifetime

229

230

16

History of stereotactic and functional neurosurgery in brazil

between Sa˜o Paulo and his ranch in Rio Grande do Sul, and still flies his ultralight plane like a young man (previously, he used to fly a Cessna 182, the skyline), despite the number of forced landings he has endured. The void left with the sudden exit of Paris Souza was filled by his prior classmate from the Medical School in Porto Alegre, Manoel Krimberg. Krimberg was formed neurosurgeon by Elyseu Paglioli at Sa˜o Jose´ Hospital. After 2 years in France with Talairach and Guiot (1963/1964), he returned to Porto Alegre, and in 1965 performed his first stereotactic procedure, a thalamotomy in a parkinsonian patient, using the Talairach apparatus. His stereotactic practice was going remarkably well until he associated with the anatomist Paolo Contu, an expert in glia. Apparently incited by Contu, as we were told (Ney Azambuja, personal communication), Krimberg started performing autologous sciatic nerve grafting to treat spinal cord injury patients, proclaiming spectacular results. Paglioli, his chief, became upset and in 1969 Krimberg left Sa˜o Jose´ Hospital and started working in two other places: Brigada Militar Hospital, in Porto Alegre, and Nossa Senhora das Grac¸as Hospital, in Canoas, in the countryside. At this point, we lost his track. We were recently told about his death years ago (uncertain date). Once again practically orphan of stereotactic and functional neurosurgery, the next in the row to restart the specialty in Porto Alegre was Telmo Tonetto Reis. Reis graduated from the Federal University of Rio Grande do Sul in 1964 and finished his neurosurgical training at Maia Filho Hospital, in Porto Alegre, in 1966. In 1967, unable to afford an air trip, and with one thousand dollars in his pocket, he endured a 15-day ship trip to London, where he spent 1 year at the National Hospital Queen Square under Valentine Logue. He then moved on to Edinburgh, where he accompanied John Gillingham and Edward Hitchcock for another year (1968). Part of this period (1 month and a

half) was spent in France with Guiot. Returning to Porto Alegre, he performed his first stereotactic procedure (thalamotomy) to treat a parkinsonian patient in 1969, by using the Guiot and Gillingham apparatus, at Moinho de Ventos Hospital. Still an active functional neurosurgeon, his main area of expertise is movement disorders. Graduated from the Federal University of Parana´ in 1974, Jose´ Vitor Pinto did his neurosurgical training at Maia Filho Hospital and Moinho de Ventos Hospital (1975/1976), in Porto Alegre, under Telmo Reis, who introduced him to stereotaxis. Enchanted with stereotactic and functional neurosurgery, Pinto decided to follow the steps of his chief. In 1977 he went to Edinburgh, spending 2 years under Edward Hitchcock and John Gillingham. In 1979, when Hitchcock moved to Birmingham, Pinto did the same, staying for another year. Returning to Porto Alegre with a Hitchcock apparatus and a Radionics radiofrequency generator in his luggage, he started his practice working with Telmo Reis at Moinho de Ventos Hospital, a partnership that still remains. In the 1980s, Pinto was probably the first to perform pallidotomy (Leksell’s target) for Parkinson’s disease in our country. His initial series of 30 cases was first presented in the XVIII Congress of the Brazilian Society of Neurosurgery in 1990. Pinto was president of the Brazilian Society for Stereotactic and Functional Neurosurgery in the biennium 1988/1990. Two other superb functional neurosurgeons started their practice in Porto Alegre before Pinto: Paulo Petry Oppitz and Ney Arthur Vilamil de Castro Azambuja. Paulo Oppitz graduated from the Catholic University of Pelotas in 1969. Some time after his 2-year neurosurgical training at Sa˜o Jose´ Hospital with Nelson Ferreira, in Porto Alegre (1970/ 1971), Oppitz went to Buenos Aires, spending 1 year with Jorge Schvarcz, and then to Edinburgh, accompanying Hitchcock for 6 months. Soon after his arrival in Edinburgh, he purchased the fifth Hitchcock apparatus sold in the world,

History of stereotactic and functional neurosurgery in brazil

which costed him five thousand pounds. In fact, Hitchcock even used Oppitz recently acquired frame in some of his operations. Returning to Porto Alegre, Oppitz started his practice at Cristo Redentor Hospital in 1976, and like almost all functional neurosurgeons of his state, his main area of expertise is the surgical treatment of movement disorders. Ney Azambuja graduated from the Catholic Medical School of Porto Alegre (now a federal foundation) in 1974, and like Oppitz, did his 3-year neurosurgical residence at Sa˜o Jose´ Hospital (1975/1977). In 1978 Azambuja went to Zurich, spending 1 year under Jean Siegfried. Before returning to Brazil, he visited Hitchcock for 1 month. Back to Porto Alegre, he started his practice at Sa˜o Jose´ Hospital in 1980. Later, Schvarcz introduced him to Oppitz, and since then they have developed an associated stereotactic practice, first at Cristo Redentor and Sa˜o Jose´ Hospitals, and later at Moinho de Ventos and Sa˜o Lucas Hospitals. Azambuja, in the beginning of the 1980s, was probably the first in Brazil to perform periaqueductal gray matter DBS for the treatment of pain. In 1985 he obtained his master degree from the Federal University of Rio Grande do Sul. As he became interested in epilepsy surgery, Azambuja moved from Sa˜o Jose´ Hospital to Sa˜o Lucas Hospital, the teaching hospital at the Pontifical Catholic University of Rio Grande do Sul, and undoubtedly one of the most renowned centers of epilepsy surgery in the country. Azambuja is now Associate Professor and regent of the discipline of neurosurgery at the Pontifical Catholic University of Rio Grande do Sul, as well as researcher of the Institute of Biomedical Research at the same institution. His main areas of expertise are the surgical treatment for epilepsy [137–139], movement disorders and pain [140], in particular trigeminal neuralgia. Other colleagues devoting part of their practice to stereotactic and functional neurosurgery in Rio Grande do Sul State are: Elyseu Paglioli Neto

16

(Porto Alegre, epilepsy surgery only), Jorge Bizzi (Porto Alegre), and Leonardo Frighetto (Passo Fundo, mainly radiosurgery).

Santa Catarina State Marcelo Neves Linhares was the pioneer of stereotactic and functional neurosurgery in Santa Catarina State, starting his practice in Floriano´polis, the state capital, in 1999. Curiously, he is still the only functional neurosurgeon in his state. Linhares graduated from the Federal University of Santa Catarina in 1992. After finishing his neurosurgical residence (1994/1997), he stayed at the USP Medical School under Teixeira for 5 months (1998), and then moved on to Toronto, doing a 1-year fellowship under Ronald Tasker and Andres Lozano (1998/1999) [141]. Linhares obtained his PhD from the USP Medical School in Ribeira˜o Preto, Sa˜o Paulo State, in 2005, and in 2007 he became Associate Professor of Neurosurgery at the Federal University of Santa Catarina.

Northeast Region The Northeast region is composed by the following states: Pernambuco, Ceara´, Bahia, Paraı´ba, Alagoas, Sergipe, Rio Grande do Norte, Maranha˜o, and Piauı´. There is a certain degree of uncertainty regarding the place, neurosurgeon and date that stereotactic and functional neurosurgery was inaugurated in the Northeast. We will try to clear this up along the next paragraphs. Manoel Caetano de Barros, the oldest Brazilian neurosurgeon still alive (sadly, Caetano de Barros died on 31 October 2008, sometime after we finished writing this chapter), was the pioneer of neurosurgery in the Northeast region of the country, starting his career in Recife, capital of Pernambuco, in 1947, initially as a self-taught neurosurgeon. Still in 1947 he went to Paris, spending 2 years with Clovis Vincent at Salpetrie`re

231

232

16

History of stereotactic and functional neurosurgery in brazil

Hospital. In 1950 he returned to Europe, this time to London, spending 1 year under McKissock at the National Hospital Queen Square. In 1958 Caetano de Barros became Full Professor of Neurosurgery and Head of the Department of Neurology and Neurosurgery at the Federal University of Pernambuco. In his service at Pedro II Hospital, at that time the teaching hospital at the Federal University of Pernambuco, there was a Talairach apparatus acquired in the 1960s. For this reason, it has been assumed that he was the pioneer also of stereotactic and functional neurosurgery in the Northeast region of the country. We tried to contact him, but he is already very old (94 years old) and unfortunately unable to answer our questions. His son, Alex Caetano de Barros, a very active neurosurgeon in Recife, was unaware if his father had any involvement with stereotactic and functional neurosurgery in the early years of his career. Many other colleagues were consulted, but none had the answer to our question. At last, after a tough search, we were able to come up with the name of the neurologist and clinical neurophysiologist Salustiano Gomes Lins, a colleague and friend of Caetano de Barros from the old days. Salustiano Lins did his training in clinical neurophysiology in Montreal, where he had the opportunity to observe a number of stereotactic procedures. Back to Recife, he incited Caetano de Barros to purchase a stereotactic frame and start performing functional neurosurgery. The stereotactic apparatus was acquired, but, according to Lins, Caetano de Barros never really started his stereotactic practice. Once cleared up the aforementioned issue, it seems to us that the pioneer of stereotactic and functional neurosurgery in the Northeast was Djacir Figueiredo, from Fortaleza, capital of Ceara´. Graduated from the Federal University of Ceara´ in 1955, Figueiredo was formed neurosurgeon by Elyseu Paglioli, in Porto Alegre (Rio Grande do Sul State), at Sa˜o Jose´ Hospital, one of the two first Brazilian neurosurgical schools. In 1964 he went to New York, spending 1 year under

Lawrence Pool at the Neurological Institute of Columbia University. During his time in the USA, Figueiredo visited Earl Walker at Johns Hopkins for 2 months, where he first became involved with stereotactic and functional neurosurgery. At that time Walker used the McKinney stereotactic instrument. Before returning to Fortaleza, Figueiredo purchased the improved version of the McKinney apparatus, and even not being a genuine functional neurosurgeon, he was the first to perform a stereotactic procedure in the Northeast. From 1965 to 1968 he operated on five parkinsonian patients, and then quit his stereotactic practice. With the vacuum left by Figueiredo, someone else wishing to dedicate to stereotactic and functional neurosurgery was needed. This space was occupied by Vicente de Paula Lobo, who worked in the team coordinated by Djacir Figueiredo. Vicente de Paula Lobo (1930–2007) graduated from the Federal University of Ceara´ in 1960 and finished his neurosurgical training at Rio de Janeiro Neurological Institute, under Jose´ Ribe Portugal, in 1963. During his residency he was first exposed to stereotactic and functional neurosurgery by Renato Barbosa. In 1972 Lobo returned to Rio de Janeiro to update his training in stereotactic and functional neurosurgery, again under Renato Barbosa, but at this time at the Lagoa Hospital, since Barbosa had already left the Neurological Institute. Returning to Fortaleza, after the acquisition of a Riechert and Mundinger apparatus, Lobo performed his first procedure for Parkinson’s disease at Fortaleza General Hospital in May 1973. Approximately in 1980, due to the pronounced declining in the surgical indication for Parkinson’s disease, Lobo also abandoned the field of stereotaxis. In 1985, Fla´vio Belmino Barbosa Evangelista, who did his residence training at the Rio Janeiro Neurological Institute under Gianni Temponi, one of the pioneers of stereotactic and functional neurosurgery in Rio de Janeiro and Brazil, started performing stereotactic surgery in Fortaleza, mainly for Parkinson’s disease and only in private clinic.

History of stereotactic and functional neurosurgery in brazil

The pioneer of stereotactic and functional neurosurgery in Pernambuco was Gla´ucio Veras. Veras trained with G. Dieckmann, in Go¨ttingen, from 1979 to 1985. Back to Brazil he stayed in Foz do Iguac¸u, Parana´, until 1989 and then moved on to Recife, capital of Pernambuco. In 1991 he inaugurated the Pain Clinic at the Cancer Hospital, and in 1993 he started performing stereotactic surgery in the same institution. His practice has been dedicated almost exclusively to pain surgery [142] and brachytherapy, having performed only a few procedures for other functional disorders. The most active functional neurosurgeon in this state, however, is Paulo Thadeu Brainer-Lima. Brainer-Lima graduated from the University of Pernambuco Medical School in 1989 and did his residence training at Restaurac¸a˜o Hospital, in Recife, from 1991 to 1994. In 1995 he went to the USP Medical School, spending 1 year and a half under Marino Jr. During this period he also had the privilege to accompany Teixeira, Cukiert, and Oliveira Jr. He then went to Oxford University (1998), staying with Tipu Aziz for 9 months. Returning to Recife, he started performing stereotactic and functional neurosurgery in 1999, and since then he has coordinated the Stereotactic and Functional Neurosurgery Service of the Division of Neurosurgery at Restaurac¸a˜o Hospital, the most important neurosurgical school in the Northeastern region. Brainer-Lima obtained his master degree in 1999, and his PhD in 2003, both from the same institution, the Federal University of Pernambuco. In September 2008, he became president of the Brazilian Society for Stereotactic and Functional Neurosurgery. The main foci of his career have been surgical treatment of pain, movement disorders and epilepsy [143–145]. Maria da Glo´ria S. Pabst was the pioneer of stereotactic and functional neurosurgery in Bahia State. Trained by Teixeira at the USP Medical School in 1991, she started her practice in Salvador (state capital) in 1992, performing her first procedure for Parkinson’s disease (helped by

16

Teixeira) in the same year. Due to a number of difficulties, however, her activities in the field have been restricted to stereotactic biopsy and stereotactic guided surgery since then. Stereotactic and functional neurosurgery in Bahia only flourished very recently (2006), though, with the arrival of Yuri Andrade-Souza in Salvador. Andrade-Souza did his neurosurgical training (1999/2002) at Sa˜o Jose´ Hospital, in Porto Alegre, under Nelson Ferreira (Ferreira, though a general neurosurgeon, was the first in Brazil to perform trigeminal retrogasserian rhizothomy by using radiofrequency thermocoagulation). In 2003 he went to the University of Toronto, spending 1 year under Andres Lozano at the Toronto Western Hospital, and 1 year and a half under Michael Schwartz at Sunnybrook Hospital. He then moved on to the University Hospital, University of Western Ontario, in London (Canada), staying 1 year under Andrew Parrent to learn epilepsy surgery. During his fellowships he published a number of significant papers [146–153]. Back to his hometown, Salvador, in 2006, Andrade-Souza has established a growing and active practice devoted to functional neurosurgery. The pioneer of stereotactic and functional neurosurgery in Paraı´ba was Valdir Delmiro Neves. Neves started his practice in the field in Joa˜o Pessoa, state capital, in 1997, after being trained by Teixeira. Some years later (2000) the colleague Ussaˆnio Mororo´ Meira [154], trained by Oliveira Jr, arrived in Joa˜o Pessoa. Both have a busy practice in the field of stereotactic and functional neurosurgery. Heider Lopes de Souza was the first to perform stereotactic and functional neurosurgery in Rio Grande do Norte. Souza did his neurosurgical training at Paulista Medical School, Federal University of Sa˜o Paulo, period in which he intermittently accompanied Teixeira at USP Medical School. He obtained his master degree in 1993, and his PhD (trigeminal neuralgia) in 2000, both from the Federal University of

233

234

16

History of stereotactic and functional neurosurgery in brazil

Sa˜o Paulo. In 1996 he started his practice in Natal, capital of the state. Se´rgio Adrian Fernandes Dantas, in 2002, was though the first neurosurgeon with formal training in stereotactic and functional neurosurgery to establish his practice in Natal. Dantas initially spent 1 year with Oliveira Jr at AC Camargo Hospital, in Sa˜o Paulo. He then went to Lille and spent two more years under Serge Blond [155]. The first neurosurgeon to perform a stereotactic procedure in Maranha˜o, more precisely in its capital, Sa˜o Luı´s, was Osmir de Ca´ssia Sampaio. Sampaio, in 1995, after a short period (2 months) with Teixeira, started performing stereotactic biopsy, but he never went beyond this. He is truly a general neurosurgeon, and just wanted to widen his surgical possibilities. The first ‘‘authentic’’ functional neurosurgeon in Maranha˜o was in fact Jose´ Roberto Pereira Guimara˜es, who started his practice in 1999 after a formal training with Oliveira Jr in Sa˜o Paulo. Reynaldo Mendes de Carvalho Jr is the pioneer and still the only functional neurosurgeon in Piauı´, having established his practice in Teresina, state capital, in 1998, after a regular training with Teixeira. Likewise, Paulo Roberto Santos Mendonc¸a, from Aracaju, the capital of Sergipe State, is the only functional neurosurgeon in his state. He trained with Oliveira Jr for 2 years and only recently (2006) started his practice. According to Abynada´ de Siqueira Lyro, the oldest neurosurgeon from Alagoas, there is no one in his state dedicated to stereotactic and functional neurosurgery; some colleagues, though, do perform stereotactic biopsy, like Ricardo Camelo and Aldo Calac¸a. Other colleagues from the Northeast performing stereotactic and functional neurosurgery to a lesser extent are: Antoˆnio Marcos de Albuquerque (Pernambuco), Ju´lio Augusto Lustosa Nogueira (Pernambuco), Joa˜o Carlos Soares de Souza Jr (Maranha˜o), Ro´dio Luiz Branda˜o Caˆmara (Rio Grande do Norte), Ricardo Rodrigues de Carvalho (Paraı´ba), and Orlando Espinheiro Freire de Carvalho Filho (Bahia).

North Region Though a vast region, the largest in the country, Para´, to the best of our knowledge, is the only state of the North region (made up by the states of Amazonas, Para´, Roraima, Rondoˆnia, Acre, Amapa´, and Tocantins) in which stereotactic and functional neurosurgery has been implanted. The first neurosurgeon to perform stereotactic and functional neurosurgery in the North region was Joffre Moreira Lima. Joffre Moreira Lima (1918–1990) graduated from the Federal University of Para´ Medical School in 1955. After finishing his neurosurgical training under Jose´ Ribe Portugal at Rio de Janeiro Neurological Institute (1956 and 1957), he returned to Bele´m, capital of Para´, becoming together with Eloy Simo˜es Bona one of the pioneers of neurosurgery in this state [2]. In the next 2 years (1958 and 1959), he returned frequently to Rio de Janeiro Neurological Institute, keeping in close touch with Portugal and Renato Barbosa, the father of stereotactic and functional neurosurgery in Brazil. While doing the research for this chapter, we were told by Ce´sar Neves, one of the most active and renowned neurosurgeons of Para´, that Joffre Lima had performed stereotactic surgery for Parkinson’s disease a long time before. The physical therapist Lila Janahu, Lima’s daughter, under our request consulted very old operative recordings of Santa Casa de Miserico´rdia de Bele´m Hospital, where her father worked, and discovered that Joffre Lima operated on a patient with epilepsy on 22 September 1958, and a patient with Parkinson’s disease on 22 July 1959. Therefore, it seems that Lima was also the pioneer of stereotactic and functional neurosurgery in Para´. Unfortunately, we could not determine for how long he kept his stereotactic practice or any other details in this regard. More recently, stereotactic and functional neurosurgery was restarted in Para´ by Scylla Lage Silva Neto. Silva Neto, during the last year of his residency in Sa˜o Paulo (1988), accompanied

History of stereotactic and functional neurosurgery in brazil

Teixeira part of the time at USP Medical School. He then moved on to Freiburg, spending 2 years (1989/1990) with Christopher Ostertag. Returning to Bele´m, Silva Neto performed his first functional procedure in March, 1991. Albedy Moreira Bastos, also trained by Teixeira, started his practice in stereotactic and functional neurosurgery in 1994. Though very experienced in the areas of pain surgery and stereotactic biopsy, and despite their adequate training, little have they done in the other areas of stereotactic and functional neurosurgery. Kleber Duarte, another disciple of Teixeira, stayed in Bele´m from 1995 to 1999. During this period he performed a variety of functional procedures, including 32 operations for Parkinson’s disease, but then he moved on to Rio de Janeiro and later to Sa˜o Jose´ do Rio Preto (Sa˜o Paulo State), where he keeps a busy practice. More recently, two other colleagues, Mauro Almeida and Jose´ Cla´udio Rodrigues, both trained by Oliveira Jr, initiated their stereotactic and functional neurosurgery practice in Bele´m.

The Brazilian Functional Neurosurgeons Abroad At present there are five Brazilian functional neurosurgeons working abroad (USA, 3; Canada, 1; and Germany, 1), three of them already well established. The first to follow this trajectory was Antonio De Salles, 25 years ago. Antonio Afonso Ferreira De Salles (Antonio De Salles) (> Figure 16-16) graduated from the Federal University of Goia´s Medical School in 1978. After his 4-year residency at Goiaˆnia Neurological Institute (1979/1982), he went to the Division of Neurosurgery at the Medical College of Virginia for a research fellowship in head injury (1983/1985), and in 1986 he got his PhD at the Virginia Commonwealth University. Both activities were supervised by Donald Becker. His primary interest was on head injury, and he

16

. Figure 16-16 Antonio Afonso De Salles

certainly made very important contributions to this field, which are beyond the scope of this chapter. After that, his interest turned to stereotactic and functional neurosurgery and he moved to Massachusetts General Hospital, Harvard Medical School, for a clinical and research fellowship under Raymond Kjellberg (1986/1988). He then spent 1.5 year at Umea University with Lauri Laitinen (1988/1989). Back to the USA, he was invited by his former boss, Donald Becker, to the UCLA School of Medicine, where he was appointed Assistant Professor, Head of the Stereotactic Surgery Section, and co-director of the radiosurgery program, positions that he still holds. In 1999 he became Full Professor at the Division of Neurosurgery and Department of Radiation Oncology at UCLA School of Medicine. His contributions to stereotactic and functional neurosurgery have been substantial. He was the first to demonstrate that low-frequency/ low-voltage electrical stimulation of the pontine parabrachial region in cats produces a nonopiate-mediated pain suppression, as well as the connections of this region with the frontal fields

235

236

16

History of stereotactic and functional neurosurgery in brazil

[156–158]. De Salles demonstrated for the first time that MRI and CT scans could be matched in the stereotactic space, which prompted the development of the image fusion technique, widely used nowadays [159]. Over the years, his team did several firsts: MR-guided radiofrequency ablation of brain tumors [160]; performance of functional neurosurgery in the MRI operating room, showing the feasibility of electrophysiological studies in such an environment [161,162]; LINAC radiosurgery for the treatment of trigeminal neuralgia [163]; demonstration of the changes in the neurotransmitters environment following low-dose LINAC radiosurgery in non-human primates, which may be implicated in the response to radiosurgery [164]; the use of shaped beam radiosurgery in a multitude of applications [165]; and the impact of ventromedial hypothalamus DBS on food intake in freely moving non-human primates [166]. Once graduated from the Paulista Medical School, Federal University of Sa˜o Paulo, in 1993, Clement Hamani did his PhD in Neurosciences in the same institution (1994/1996), under Luiz Mello, studying the reorganization of hippocampal circuitry in a pilocarpine-induced rat model of epilepsy [167,168]. During this period, he spent 8 months at the University of Illinois in Chicago as a research fellow, working with microdialysis in the brain [169]. From 1997 to 2002, he did his residence training at the USP Medical School, under Raul Marino Jr, and after a 6-month fellowship in functional neurosurgery with Manoel Teixeira, in the same institution, he went to the University of Toronto, where, under the supervision of Andres Lozano, he did his postdoctorate fellowship. In 2005 he became Invited Professor (neurophysiology) of the Federal University of Sa˜o Paulo. In 2007, he was offered the position of Associate Researcher of the Center of Addiction and Mental Health of the University of Toronto, and in July, 2008, became Assistant Professor, Division of Neurosurgery, Toronto Western Hospital, of this great university. As a member of Andres Lozano’s team, he has been part of a

number of very important researches, both clinical and laboratorial, such as subgenual cingulum DBS for depression [106], anterior thalamic nucleus DBS for epilepsy [170,171], hypothalamic/ fornix DBS for memory enhancement [172], and pedunculopontine nucleus DBS for progressive supranuclear palsy and Parkinson’s disease [173], among others [147,148,174–180]. After finishing his residency (1998/2002) and preceptorship (2003/2004) at the University of Sa˜o Paulo Medical School, under Raul Marino Jr, Andre´ Machado did a 2-year fellowship at the Center of Neurological Restoration, Department of Neurosurgery, Cleveland Clinic, under the supervision of Ali Rezai, and since then he became a staff member of the same institution. He runs a lab at the Cleveland Clinic Lemer Research Institute focused on motor rehabilitation in animal models of stroke [181]. As part of Ali Rezai’s team, he has greatly contributed to clinical researches in motor cortex [182] and gasserian ganglion [183] stimulation for pain, DBS for movement disorders [184,185] and psychiatric illnesses [186,187], and thalamic stimulation for minimally conscious state [188]. The two other colleagues working abroad are Alessandra Gorgulho and Guilherme Lepski. Gorgulho attended a 1-year fellowship with Teixeira, in Sa˜o Paulo, and a 3-year research fellowship with the Salles, at UCLA. At present, she is an assistant researcher at the Stereotactic Surgery Section at UCLA, but is still not working as a functional neurosurgeon. Lepski, of German origin, an ex-fellow and assistant to Teixeira, in Sa˜o Paulo, has just recently (October 2007) moved to Tu¨bingen, and is now working at the University of Eberhard-Karls under Marcos Tatagiba.

The Brazilian Society for Stereotactic and Functional Neurosurgery Despite its constant growth, the Brazilian Society of Neurosurgery (Sociedade Brasileira de

History of stereotactic and functional neurosurgery in brazil

Neurocirurgia – SBN) started to be departmentalized into its various subspecialties only in 1992, during the presidency of Carlos Batista Alves de Souza. The history of Brazilian stereotactic and functional neurosurgery, however, is somewhat different from the other neurosurgical subspecialties. It started as an independent society, although connected to the SBN. After the departmentalization of SBN, it also became its Department of Functional Surgery and Pain. During the 13th Brazilian Congress of Neurosurgery, chaired by Laelio Lucas and held in Guarapari, Espı´rito Santo State, by initiative of Carlos Telles, who had recently arrived from Germany after a 4-year fellowship, the Brazilian Society for Stereotactic and Functional Neurosurgery was founded on 16 September 1980. Before the conference, Telles had written to colleagues around the country who were dealing with functional neurosurgery and invited them for a meeting dedicated to the foundation of the Brazilian Society for Stereotactic and Functional Neurosurgery. The following colleagues attended the meeting, becoming founding members of the Brazilian Society for Stereotactic and Functional Neurosurgery: Renato Barbosa, Jose´ Barros, Alceu Correia, Bernardo Couto, Djacir Figueiredo, Lourenc¸o de Freitas Neto, Nilton Latuf, Raul Marino Jr, Luiz Fernando Martins, Pedro Motta, Delfim Nunes Neto, Sergio Ottoni, Jorge Pagura, Otoı´de Pinheiro, Jose´ Vitor Pinto, Telmo Reis, Manoel Teixeira, Carlos Telles, and Gianni Temponi. Blaine Nashold Jr and Edward Hitchcock, invited speakers to the Brazilian Congress, were also present, and thankful to the invaluable support lent by Nashold, the Brazilian Society for Stereotactic and Functional Neurosurgery became affiliated to the World Society for Stereotactic and Functional Neurosurgery since its birth. Renato Barbosa, Raul Marino Jr, Carlos Telles, Otoı´de Pinheiro, and Jose´ Barros were elected, respectively, as president, vice-president, secretary, assistant secretary, and treasurer of the first board of directors of our Society. Although there

16

is some controversy about to whom should be attributed the initiative to create Brazilian Society for Stereotactic and Functional Neurosurgery, the data here reported were collected from the blotter of Brazilian Society for Stereotactic and Functional Neurosurgery. The leadership of the Brazilian Society for Stereotactic and Functional Neurosurgery is renewed every 2 years, and the following were the presidents from its birth up to now: 1980/ 1982, Renato Barbosa; 1982/1984, Raul Marino Jr; 1984/1986, Luiz Fernando Martins; 1986/ 1988, Carlos Telles; 1988/1990, Jose´ Vitor Pinto; 1990/1992, Manoel Teixeira; 1992/1994, Sebastia˜o Gusma˜o; 1994/1996, Alceu Correia; 1996/ 1998, Cla´udio Correˆa; 1998/2000, Manoel Teixeira; 2000/2002, Luiz Fernando Martins; 2002/ 2004, Jorge Pagura; 2004/2006, Edvaldo Cardoso; 2006/2008, Osvaldo Vilela Filho; and 2008/2010, Paulo Brainer-Lima. The main focus of Brazilian Society for Stereotactic and Functional Neurosurgery has always been educational. Approximately three or four meetings are organized every year, usually as a parallel activity within another greater meeting such as those of the Brazilian Society of Neurosurgery, Brazilian Academy of Neurosurgery, SIMBIDOR – Brazilian Symposium and International Meeting on Pain, and CINDOR – Interdisciplinary Congress on Pain. Besides, every 2 years, in Sa˜o Paulo, there is a meeting co-organized by Brazilian Society for Stereotactic and Functional Neurosurgery and Micromar. The first time the Brazilian Society for Stereotactic and Functional Neurosurgery organized a completely independent meeting, was on 16–19 May 2007, the 1st International Joint Meeting on Stereotactic and Functional Neurosurgery & 8th Congress of the Brazilian Society for Stereotactic and Functional Neurosurgery: The Future Today!, held at Rio Quente Resorts, Rio Quente, Goia´s State, and chaired by Osvaldo Vilela Filho, president of the Brazilian Society for Stereotactic and Functional Neurosurgery. The conference venue, with its hot springs, was magnificent, the

237

238

16

History of stereotactic and functional neurosurgery in brazil

scientific level was the highest possible, and the social activities were superb. The faculty was made up by 42 speakers, 18 from Brazil and 24 from other countries (US, Canada, Mexico, France, Italy, Sweden, China, Argentina, Chile, Venezuela, and Colombia), all well-known functional neurosurgeons. The Brazilian Society for Stereotactic and Functional Neurosurgery did not fund any speaker. Everyone graciously accepted to come on their own, in a gesture of great consideration and friendship never to be forgotten. The official clothing was casual wear, being suits and ties officially prohibited, which was instrumental in establishing a very informal atmosphere. The great innovation of the meeting was the ‘‘spicy-session,’’ in which controversial topics were fully debated by experts in an attempt to reach a consensus. One hundred and forty three participants attended the meeting, half from Brazil and half from various other countries. The Brazilian Society for Stereotactic and Functional Neurosurgery paid homage to two friends and colleagues, Ronald Tasker, International Honored President, and Luiz Fernando Martins, Brazilian Honored President, for their invaluable contributions to, respectively, world and Brazilian stereotactic and functional neurosurgery. Finally, by initiative of Eduardo Barreto and Osvaldo Vilela Filho, there was a session during the meeting, coordinated by Elliot Krames, president of the International Neuromodulation Society (INS), destined to the foundation of the Brazilian Neuromodulation Society, the Brazilian chapter of the INS, which happened on 18 May 2007. Its first board of directors was then elected: Eduardo Barreto, president; Osvaldo Vilela Filho, vice-president; and Alexandre Francisco, secretary. The Brazilian Society for Stereotactic and Functional Neurosurgery has 98 active members (85 are adequately formed functional neurosurgeons, nine of which are either currently inactive or never performed functional neurosurgery, and 13 are non-functional neurosurgeons or

neurologists) and five honorary members, who were chosen based on their great contribution to the field and relationship with Brazilian functional neurosurgeons: Ronald Tasker, Antoˆnio de Salles, Edward Hitchcock, Blaine Nashold Jr, and Wolfhard Winkelmu¨ller. Besides, there are 61 other neurosurgeons performing at least some of the stereotactic and/or functional procedures, like epilepsy alone or pain surgery and stereotactic biopsy, which gives a total of 137 (98–9–13 = 76 + 61 = 137) neurosurgeons at least partially involved with functional neurosurgery (stereotactic biopsy alone was not considered), as shown in > Figure 16-17. However, only 60 Brazilian neurosurgeons (41 members and 19 non-members) are truly functional neurosurgeons, that is, most of their practice is dedicated to stereotactic and functional neurosurgery. Finally, also worth mentioning is the creation of the Brazilian Society for the Study of Pain, which happened on 29 August 1983, by initiative of the functional neurosurgeon Jorge Pagura and the neurologist Moacir Schnapp. One year later it was affiliated to the International Association for the Study of Pain. Pagura became its second president, in fact the only functional neurosurgeon elected for president of this society.

Non-Medical Contributors for the Development of Stereotactic and Functional Neurosurgery in Brazil Until 1985, with the exception of the stereotactic frames built by the neurosurgeons Jose´ Barros and Jose´ Zaclis for their own use, all other stereotactic apparatuses in the country were imported, at a very high cost, being those of Riechert-Mundinger and Hitchcock the most commonly found. In 1985, the engineer Antonio Martos (CEO of Micromar), with the supervision of Manoel Teixeira, built the first commercially available Brazilian stereotactic apparatus,

History of stereotactic and functional neurosurgery in brazil

16

. Figure 16-17 Distribution of Brazilian neurosurgeons performing functional procedures per regions and states

. Figure 16-18 Micromar radiofrequency generator

the Micromar stereotactic system, a modification of that of Hitchcock’s. Since then, this frame has been continuously refined, achieving a very high quality. Micromar is still the only Brazilian company dedicated to the stereotactic field.

It was also very instrumental to this field manufacturing electrode kits for the different neurosurgical procedures, radiofrequency generators (the first version, released in 1996, was basically analogical and received a series of refinements along the years; in 2008, an entirely digital version was released) (> Figure 16-18), and the radiosurgery system for linear accelerator (its production was again supervised by Manoel Teixeira, being released for clinical use in 1998). Another very important person in this regard has been the physicist Armando Alaminos Bouza, with a master degree in neurosciences. He was the one responsible for the development of the software (MNPS) used in association with the Micromar stereotactic system and Micromar radiosurgery system, allowing the determination of stereotactic coordinates, detailed planning of the electrode trajectory, overlaying CT and MR

239

240

16

History of stereotactic and functional neurosurgery in brazil

. Figure 16-19 Neuroaugmentative procedures performed in Brazil from 2002 to 2008. SCS = spinal cord stimulation; DBS = deep brain stimulation; MCS = motor cortex stimulation; VNS = vagal nerve stimulation

images with digitized maps of stereotactic atlas (Schaltenbrand & Wahren and Talairach), shrunk or stretched as necessary to match the patient’s intercomissural distance, multimodality image fusion, and planning for radiosurgery and brachytherapy. Also important for the development of the stereotactic field in our country were Sandra Ferraz and Victor Dabah, from Dabasons Importac¸a˜o, Exportac¸a˜o e Come´rcio Ltda, local representative of Medtronic, and Joaquim Cordeiro and Ma´rcio Sossai, from JM Come´rcio e Importac¸a˜o Ltda, local representative of ANS, for their role in directly or indirectly (through neurosurgeons) spreading the reasoning for the use of neuroaugmentative techniques across the country and sponsoring the stereotactic and functional neurosurgery meetings. Sandra Ferraz should also be accounted for tirelessly backing the functional neurosurgeons in their fight against the health insurance companies in an attempt to make them pay for the procedures and necessary hardware. The results of their combined efforts can be better appreciated in > Figure 16-19, which shows a significant increase in the number of neuromodulatory procedures in our country.

Recent developments will most probably change forever this panorama, strengthening the tendency shown in > Figure 16-19. Until recently, neuromodulatory surgeries were not officially recognized by the National Health Agency (Ageˆncia Nacional de Sau´de – ANS). On 2 April 2008, though, according to the normative resolution number 167 of ANS, published in the Official Diary of the Union, neuroaugmentative surgeries became part of the roll of procedures recognized by ANS, which means that, from now on, private health insurance companies will be obliged to authorize and pay for these procedures. The Brazilian functional neurosurgical community will always be in great debt to all these people.

Acknowledgments Besides those already mentioned in the introductory part of the chapter, the author would like to express his deep gratitude to Fernanda Vilela for proofreading this manuscript.

History of stereotactic and functional neurosurgery in brazil

References 1. Horrax G. Neurosurgery: a historical sketch. Springfield, IL: Thomas; 1952. p. 10-15. 2. Gusma˜o SS, de Souza JG. Histo´ria da Neurocirurgia no Brasil [History of Brazilian neurosurgery]. Joinville: Letra Me´dica; 2000. 3. Souza APS, Vale´rio AG. A cirurgia nervosa no Brasil [Neurological surgery in Brazil]. Anais do Segundo Congresso Brasileiro de Neurologia-Psychiatria e Medicina Legal. Arch Neurol Psiq e Med Legal 1922;6:30-67. 4. Mario Brock. Jose´ Ribeiro Portugal. J Bras Neurocir 2008;19(1):38-41. 5. Coutinho MF. Obitua´rio: Renato Tavares Barbosa. J Bras Neurocir 2003;14(1):29. 6. Livro de atas da Sociedade Brasileira de Neurocirurgia Funcional e Estereota´xica (Blotter of the Brazilian Society for Stereotactic and Functional Neurosurgery). 7. Filho PN. Paulo Niemeyer. Arq Bras Neurocir 2004;23 (1):8-11. 8. Yacubian EM, Cavalheiro EA. In memoriam: Paulo Niemeyer Soares. Epilepsia 2004;45(9):1166-8. 9. Niemeyer P. Tratamento ciru´rgico do tremor parkinsoniano, da atetose e outras hipercinesias. Med Cirurg Farm 1945;116:1-16. 10. Niemeyer P. Tratamento ciru´rgico das discinesias. Rev Bras Cir 1955;30(4):211-48. 11. Niemeyer P. Supressa˜o da resposta motora e da atividade cortical ele´trica no homem. Arq Neuropsiquiatr 1946;4:109-17. 12. Niemeyer P. The transventricular amygdala-hippocampectomy in temporal lobe epilepsy. In: Baldwin MBP, editor. Temporal lobe epilepsy. Springfield, IL: Thomas; 1958. p. 461-82. 13. Cendes F, Dubeau F, Olivier A, Cukiert A, Andermann E, Quesney LF, et al. Increased neocortical spiking and surgical outcome after selective amygdalo-hippocampectomy. Epilepsy Res 1993;16(3):195-206. 14. Lynch JC. Gianni Maure´lio Temponi (1934–2007). Boletim da SBN (SBN Newsletter). Outubro; 2007. p. 22. 15. Temponi G. Estudo sobre 100 intervenc¸o˜es estereota´xicas cerebrais no tratamento do parkinsonismo (Abstr.). In: Mattos Pimenta A, editor. XI Congresso Latino-Americano de Neurocirurgia (Relato´rios Oficiais e Comunicac¸o˜es Livres), Sa˜o Paulo; 1965. p. 272. 16. Telles CR. Nova te´cnica para o tratamento das algias cervicofaciais neopla´sicas. Presented at the 14th Brazilian Congress of Neurosurgery, Belo Horizonte, Sept 1982. 17. Telles CR. Tratamento ciru´rgico das dores cervicofaciais de origem neopla´sica. Presented at the 20th Latin American Congress of Neurosurgery, Sa˜o Paulo, Mar 1983. 18. Telles CR. Facial pain due to cancer of head and neck. Presented at the Annual Meeting of the American Society for Stereotactic and Functional Neurosurgery, North Caroline, Apr 1983. 19. Aloysio Mattos Pimenta. Curriculum Vitae, 1959.

16

20. Yahn M, Mattos Pimenta A, Sette A, Jr. Tratamento ciru´rgico das mole´stias mentais (Leucotomia), Sa˜o Paulo; 1951. 21. Mattos Pimenta A. XI Congresso Latino-Americano de Neurocirurgia (Relato´rios Oficiais e Comunicac¸o˜es Livres). Sa˜o Paulo; 1965. 22. Barros NG. In memoriam: Jose´ Zaclis (1917–1983). Arq Neuropsiquiatr 1984;42:84-5. 23. Zaclis J. [X-ray visualization of the entire cerebrovascular system by means of contrast medium injection into one single artery; cerebral pan-angiography.] Arq Neuropsiquiatr 1959;17(1):1-22. (Portuguese). 24. Zaclis J, Longo PH, Cruz OR. Intrathoracic hyperpressure in neuroradiology; results in (1) cerebral panangiography and (2) arteriography of the thoracocervical region. J Neurosurg 1964;21:1087-94. 25. Zaclis J, Koralek JM, Longo PH, Almeida GM. Novo aparelho para neurocirurgia estereota´xica (Abstr.). In: Mattos Pimenta A (Ed). XI Congresso Latino-Americano de Neurocirurgia Sa˜o Paulo; (Relato´rios Oficiais e Comunicac¸o˜es Livres). 1965. p. 272. 26. Marino R. Jr. Reflections on a stereotactic and functional journey: the blessing and inspiration of working among giants. Neurosurgery 2005;56(1):172-7. 27. Ballantine HT, Jr, Cassidy WL, Flanagan NB, Marino R, Jr. Stereotaxic anterior cingulotomy for neuropsychiatric illness and intractable pain. J Neurosurg 1967;26 (5):488-95. 28. Cassidy WL, Ballantine HT, Jr, Flanagan NB. Frontal cingulotomy for affective disorders. Recent Adv Biol Psychiatry 1965;8:269-82. 29. Rasmussen T, Marino R, Jr. Functional neurosurgery. New York: Raven Press; 1978. 30. Ragazzo PC, Manzano GM, Marino R, Jr. Functional microsurgical partial callosotomy in patients with secondary generalized epilepsies. I. Disruption of bilateral synchrony of spike and wave discharges. Appl Neurophysiol 1988;51(6):297-306. 31. Marino Ju´nior R, Gronich G. Corpus callosum stimulation and stereotactic callosotomy in the management of refractory generalized epilepsy. Arq Neuropsiquiat 1989;47(3):320-5. 32. Marino Ju´nior R. Surgery for epilepsy. Selective partial microsurgical callosotomy for intractable multiform seizures: criteria for clinical selection and results. Appl Neurophysiol 1985;48(1–6):404-7. 33. Cukiert A, Puglia P, Scapolan HB, Vilela MM, Marino Ju´nior R. Congruence of the topography of intracranial calcifications and epileptic foci. Arq Neuropsiquiatr 1994;52(3):289-94. 34. Marino Ju´nior R, Cosgrove GR. Neurosurgical treatment of neuropsychiatric illness. Psychiatr Clin North Am 1997;20(4):933-43. 35. Wen HT, Rhoton AL, Jr, Marino R, Jr. Anatomical landmarks for hemispherotomy and their clinical application. J Neurosurg 2004;101(5):747-55.

241

242

16

History of stereotactic and functional neurosurgery in brazil

36. de Almeida AN, Marino R, Jr. The early years of hemispherectomy. Pediatr Neurosurg 2005;41(3): 137-40. 37. Wen HT, Rhoton AL, Jr, Marino R, Jr. Gray matter overlying anterior basal temporal sulci as an intraoperative landmark for locating the temporal horn in amygdalohippocampectomies. Neurosurgery 2006;59 (4 Suppl 2):ONS221-7. 38. Teixeira MJ. Various functional procedures for pain. Part II: Facial pain. In: Gildenberg PL, Tasker RR, editors. Textbook of stereotactic and functional neurosurgery. New York: McGraw-Hill; 1998. p. 1389-402. 39. Teixeira MJ, Lepski G, Aguiar PH, Cescato VA, Rogano L, Alaminos AB. Bulbar trigeminal stereotactic nucleotractotomy for treatment of facial pain. Stereotact Funct Neurosurg 2003;81(1–4):37-42. 40. Hitchcock E. Stereotactic trigeminal tractotomy. Farmatsiia 1970;19(3):131-5. 41. Hitchcock E, Teixeira MJ. Pontine stereotactic surgery and facial nociception. Neurol Res 1987;9(2):113-7. 42. Fonoff ET, Dale CS, Pagano RL, Paccola CC, Ballester G, Teixeira MJ, et al. Antinociception induced by epidural motor cortex stimulation in naive conscious rats is mediated by the opioid system. Behav Brain Res (2008). doi:10.1016/j.bbr.2008.07.027. 43. Fonoff ET, Dale CS, Pagano RL, Teixeira MJ, Ballester G, Giorgi R. Antinociceptive effect induced by sensorimotor cortex stimulation in normal rats. Young Investigator Award. Presented at the 14th Meeting of the World Society for Stereotactic and Functional Neurosurgery, Rome, Italy, June 2005. 44. Teixeira MJ, Fonoff ET, Montenegro MC. Dorsal root entry zone lesions for treatment of pain-related to radiation-induced plexopathy. Spine 2007;32(10): E316-9. 45. Teixeira MJ, Fonoff ET, Macri F, Picarelli H, Lin TY, Marcolin MA. Prediction of Motor Cortex Simulation in Treatment of Brachial Plexus Avulsion Pain by Transcranial Magnetic Stimulation. NeuPSIG Poster Prize (category: clinical studies) presented at the Second International Congress on Neuropathic Pain, Berlin, Germany, June 2007. 46. de Almeida AN, Fonoff ET, Ballester G, Teixeira MJ, Marino R, Jr. Stereotactic disconnection of hypothalamic hamartoma to control seizure and behavior disturbance: case report and literature review. Neurosurg Rev 2008;31 (3):343-9. 47. Fonoff ET, Lara N, Teixeira MJ. Phrenic nerve stimulation for the treatment of refractory hiccup. Presented at the Meeting of the European Society for Stereotactic and Functional Neurosurgery, Rimini, Italy, Oct 2008. 48. Teixeira MJ, Fonoff ET, Santana PA, Padilha PM, Cescato VAS. Computer-assisted stereotactic fenestration of aqueductal cyst for treatment of hydrocephalus: a technical report. Presented at the, 14th Meeting of the World Society for Stereotactic and Functional Neurosurgery, Rome, Italy, June 2005.

49. Cescato VAS, Teixeira MJ, No´brega, JPS, Almeida GM, Oliveira JO, Jr., Butori S. Tratamento de granuloma blastomico´tico cı´stico talaˆmico por meio de instilac¸a˜o estereota´xica de quimiotera´picos atrave´s de caˆnula intralesional. Presented at the XVI Brazilian Congress of Neurosurgery, Rio de Janeiro, Brazil, Sept 1986. 50. Hitchcock ER, Teixeira MJ. A comparison of results from center-median and basal thalamotomies for pain. Surg Neurol 1981;15(5):341-51. 51. Teixeira MJ, De Souza EC, Yeng LT, Pereira WC. [Lesion of the Lissauer tract and of the posterior horn of the gray substance of the spinal cord and the electrical stimulation of the central nervous system for the treatment of brachial plexus avulsion pain]. Arq Neuropsiquiatr 1999;57 (1):56-62. (Portuguese). 52. Teixeira MJ, Lepski G, Correia C, Aguiar PH. Interstitial irradiation for CNS lesions. Stereotact Funct Neurosurg 2003;81(1–4):24-9. 53. Rogano L, Teixeira MJ, Lepski G. Chronic pain after spinal cord injury: clinical characteristics. Stereotact Funct Neurosurg 2003;81(1–4):65-9. 54. Rogano LA, Greve JM, Teixeira MJ. Use of intrathecal morphine infusion for spasticity. Arq Neuropsiquiatr 2004;62(2B):403-5. 55. de Siqueira SR, da No´brega JC, de Siqueira JT, Teixeira MJ. Frequency of postoperative complications after balloon compression for idiopathic trigeminal neuralgia: prospective study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006;102(5):e39-45. 56. Arantes PR, Cardoso EF, Barreiros MA, Teixeira MJ, Gonc¸alves MR, Barbosa ER, et al. Performing functional magnetic resonance imaging in patients with Parkinson’s disease treated with deep brain stimulation. Mov Disord 2006;21(8):1154-62. 57. Teixeira MJ, de Siqueira SR, Bor-Seng-Shu E. Glossopharyngeal neuralgia: neurosurgical treatment and differential diagnosis. Acta Neurochir (Wien) 2008;150 (5):471-5. 58. de Almeida AN, Teixeira MJ, Feindel WH. From lateral to mesial: the quest for a surgical cure for temporal lobe epilepsy. Epilepsia 2008;49(1):98-107. 59. Pagura JR. Percutaneous radiofrequency spinal rhizotomy. Appl Neurophysiol 1983;46(1–4):138-46. 60. Pagura JR, Rabello JP, Lima WC. Microvascular decompression for trigeminal neuralgia. In: Gildenberg PL, Tasker RR, editors. Textbook of stereotactic and functional neurosurgery. New York: McGraw-Hill; 1998. p. 1715-21. 61. Pagura JR, Schnapp M, Passarelli P. Percutaneous radiofrequency glossopharyngeal rhizotomy for cancer pain. Appl Neurophysiol 1983;46(1–4):154-9. 62. Correˆa CF, Teixeira MJ. Balloon compression of the Gasserian ganglion for the treatment of trigeminal neuralgia. Stereotact Funct Neurosurg 1998;71(2):83-9. 63. Marino R, Jr., Cukiert A, Pinho E. Epidemiological aspects of epilepsy in Sa˜o Paulo, Brazil. A prevalence rate study. In:

History of stereotactic and functional neurosurgery in brazil

64.

65.

66.

67.

68.

69.

70.

71. 72.

73.

74. 75.

76.

77.

78.

Wolf P, Dam M, Janz D, Dreifuss FE, editors. Advances in epileptology. New York: Raven Press; 1987. p. 759-64. Cukiert A, Baumel SW, Andrioli MSD, Marino R, Jr. Effects of corpus callosum stimulation on the morphology and frequency of the epileptic bursts in the feline topical penicillin generalized model. Stereotact Funct Neurosurg 1989;52:18-25. Cendes F, Dubeau F, Olivier A, Cukiert A, Andermann E, Quesney LF, et al. Increased neocortical spiking and surgical outcome after selective amygdalo-hippocampectomy. Epilepsy Res 1993;16(3):195-206. Olivier A, Germano I, Cukiert A, Peters T. Frameless stereotaxy for surgery of the epilepsies: preliminary experience. Technical note. J Neurosurg 1994;81:629-33. Cukiert A, Burattini JA, Machado E, Sousa A, Vieira JO, Argentoni M, et al. Results of surgery in patients with refractory extratemporal epilepsy with normal or nonlocalizing magnetic resonance findings investigated with subdural grids. Epilepsia 2001;42:889-94. Cukiert A, Burattini JA, Machado E, Sousa A, Vieira JO, Forster C, et al. Seizure-related outcome after corticoamygdalohippocampectomy in patients with refractory temporal lobe epilepsy and mesial temporal sclerosis evaluated by magnetic resonance alone. Neurosurg Focus 2002;13(4): ecp2 Beraha J, Barcia Salorio JL, Bordes V, Hernandez G. Radiocirurgia estereota´xica./Stereotaxic radiosurgery. Arq Bras Neurocir 1984;3(1):15-22. Beraha J, Feriancic CV, Scaff LA. [Stereotaxic radiosurgery in the treatment of cerebral arteriovenous malformations]. Arq Neuropsiquiatr 1987;45(4):391-6. In memoriam: Dr. Nilton Luiz Latuf (1937–2005). Boletim da SBN (SBN Newsletter). Dezembro; 2005. Siqueira JM. A method for bulbospinal trigeminal nucleotomy in the treatment of facial deafferentation pain. Appl Neurophysiol 1985;48(1–6):277-80. Nashold BS, Jr, Caputti F, Bernard E. Trigeminal DREZ: Caudalis nuclear lesions for relief of facial pain (Abstr). Neurosurgery 1986;19(1):150. Schvarcz JR. Trigeminal DREZ (correspondence to the editor). Neurosurgery 1987;20(2):348. Gorecki JP. Dorsal root entry zone and brainstem ablative procedures. In: Winn HR, editor. Youmans neurological surgery. 5th ed. Philadelphia, PA: Saunders; 2004. p. 3045-58. Tasker RR, Siqueira J, Hawrylyshyn P, Organ LW. What happened to VIM thalamotomy for Parkinson’s disease? Appl Neurophysiol 1983;46(1–4):68-83. Tasker RR, DeCarvalho GTC, Dolan EJ. Intractable pain of spinal cord injury: clinical features and implications for surgery. J Neurosurg 1992;77:373-8. Tasker RR, de Carvalho G, Dostrovsky JO. The history of central pain syndromes, with observations concerning pathophysiology and treatment. In: Casey KL, editor. Pain and central nervous system disease: the central pain syndromes. New York: Raven Press; 1991. p. 31-58.

16

79. Tasker RR, De Carvalho GTC. Central pain of spinal cord injury. In: North RB, Levy RM, editors. Neurosurgical management of pain. New York: Springer; 1997. p. 110-6. 80. Tasker RR, DeCarvalho GC, Li CS, Kestle JRW. Does thalamotomy alter the course of Parkinson’s disease? Adv Neurol 1996;69:563-83. 81. Gusma˜o S, Oliveira M, Tazinaffo U, Honey CR. Percutaneous trigeminal nerve radiofrequency rhizotomy guided by computerized tomography fluoroscopy. Technical note. J Neurosurg 2003;99(4):785-6. 82. Martins LF, Umbach W. Simple determination of the foramen in trigeminus coagulation. Neurochirurgia (Stuttg) 1975;18(5):163-6. 83. Martins LF, Umbach W. [Clinico-anatomical correlation between sighting of the lesion and alleviation of pain following stereotactic surgery]. Neurochirurgia (Stuttg) 1974;17(3):77-83. (German). 84. Martins LF, Umbach W. Size and position of stereotaxic lesions in comparison with clinical pain relief. Confin Neurol 1975;37(1–3):80-5. 85. Damasceno BP, Campos Junior SS, Martins LF, de Melo-Souza SE. [Clinical treatment of resistant epilepsy]. Arq Neuropsiquiatr 1988;46(4):351-8. (Portuguese). 86. Cendes F, Ragazzo PC, da Costa V, Martins LF. [Interhemispheric disconnection syndrome following total callosotomy associated to anterior commissurotomy for the treatment of intractable epilepsy: a case report]. Arq Neuropsiquiatr 1990;48(3):385-8. (Portuguese). 87. Cendes F, Ragazzo PC, da Costa V, Martins LF. Corpus callosotomy in treatment of medically resistant epilepsy: preliminary results in a pediatric population. Epilepsia 1993;34(5):910-7. 88. Zaccariotti VA, Martins LF, da Costa V, Silva NA, da Casas AA, de Melo-Souza SE. [Sneddon syndrome. Report of 3 cases]. Arq Neuropsiquiatr 1995;53(1):82-7. (Portuguese). 89. Vilela Filho O. Estrate´gia para a abordagem de leso˜es intracranianas. Rev Goiana de Medicina 1989;35:59-70. 90. Vilela Filho O, Rocha JCN, Almeida WC, Leite MSB, Silva DJ, Cavalcante JE. Bio´psia de leso˜es intracranianas a ma˜o livre assistida por tomografia computorizada ou ultra-sonografia. Arq Bras Neurocir 1991;10(2):103-19. 91. Tasker RR, Vilela Filho O. Deep brain stimulation for neuropathic pain. Stereotact Funct Neurosurg 1995;65 (1–4):122-4. 92. Tasker RR, Vilela Filho O. Deep brain stimulation for the control of intractable pain. In: Youmans JR, editor. Neurological surgery. 4th ed. Philadelphia, PA: Saunders; 1996. p. 3512-27. 93. Vilela Filho O. Risk factors for unpleasant paresthesiae induced by parethesiae-producing deep brain stimulation. Arq Neuropsiquiatr 1996;54(1):57-63. 94. Vilela Filho O. Risk factors for paresthesia-producing deep brain stimulation (Abstr.). Resumos de poˆsteres do 3
Simpo´sio Internacional de Dor (Simbidor). Sa˜o Paulo; p. 19-20.

243

244

16

History of stereotactic and functional neurosurgery in brazil

95. Rezai AR, Francisco AN, Vilela Filho O, Lozano AM, Tasker RR. Deep brain stimulation for intractable neuropathic pain: contemporary management and outcome in 80 patients (Abstr.). J Neurosurg 1998;88:416A. 96. Vilela Filho O, Tasker RR. ‘‘Pathways involved in thalamic ventrobasal stimulation for pain relief: evidence against the hypothesis VB stimulation ! rostroventral medulla excitation ! dorsal horn inhibition’’. Arq Neuropsiquiatr 1994;52(3):386-91. 97. Vilela Filho O. Thalamic ventrobasal stimulation for pain relief: probable mechanisms, pathways and neurotransmitters. Arq Neuropsiquiatr 1994;52(4): 578-84. 98. Vilela Filho O. Pathophysiology of the steady burning, dysesthetic component of neuropathic pain: a hypothesis (Abstr). Stereotact Funct Neurosurg 2001;77:205. 99. Vilela Filho O. Tratamiento Neuroquiru´rgico del Dolor: Estado Actual. Neurotarget 2006;1(2):6-20. 100. Vilela Filho O, Correˆa CF. Dor e neuroestimulac¸a˜o: Estimulac¸a˜o ele´trica do sistema nervoso para o manejo da dor croˆnica intrata´vel. Biotecnologia 1998;6:56-66. 101. Vilela Filho O, Correˆa CF. Tratamento da dor croˆnica refrata´ria por neuroestimulac¸a˜o. Neurocirurgia Contemporaˆnea Brasileira 1999;2(12): 1–8. 102. Vilela Filho O, Araujo MR, Florencio RS, Silva MAC, Silveira MT. CT-guided percutaneous punctate midline myelotomy for the treatment of intractable visceral pain: technical note. Stereotact Funct Neurosurg 2001;77: 177-82. 103. Vilela Filho O, Pereira CE. Establishment of a reliable landmark to guide percutaneousradiofrequency occipital neurotomy (Abstr). Stereotact Funct Neurosurg 2001;77:204. 104. Vilela Filho O. In vivo evaluation of cordotomy lesions by magnetic resonance imaging: a new approach (Abstr). Stereotact Funct Neurosurg 2001;77:203-4. 105. Vilela Filho O, Carneiro Filho O, Souza HAO, Machado DC, Rodrigues Filho S, Campos JA. SPECT-based tailoring of psychosurgical procedures: is it possible? Stereotact Funct Neurosurg 2001; 76:256-61. 106. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C, et al. Deep brain stimulation for treatment-resistant depression. Neuron 2005;45 (5):651-60. 107. Franzini A, Ferroli P, Leone M, Broggi G. Stimulation of the posterior hypothalamus for treatment of chronic intractable cluster headaches: first reported series. Neurosurgery 2003;52(5):1095-9. 108. Vilela Filho O, Souza JT. Sı´ndrome de Tourette: uma decorreˆncia da hiperatividade do pa´lido lateral? Rev Psiquiat Clin 1996;22(4):138 (Abstr.). 109. Vilela Filho O, Souza JT. Sı´ndrome de Tourette: Anatomofisiologia dos gaˆnglios da base e sistema lı´mbico,

110.

111.

112.

113.

114.

115.

116.

117.

118.

119.

120.

circuita´ria e fisiopatologia. In: Santos MGP, editor. Sı´ndrome de Gilles de la Tourette: tiques nervosos e transtornos de comportamento associados na infaˆncia e adolesceˆncia. Sa˜o Paulo: Lemos Editorial; 1998. p. 137-58. Vilela Filho O, Ragazzo PC, Silva DJ, Souza JT, Oliveira PM, Carneiro Filho O, et al. Globus Pallidus externus (GPe) deep brain stimulation (DBS) for the treatment of Tourette Syndrome (TS): evaluation of a new target in a prospective Controlled Study (Abstr.). In Abstract Book of the ASSFN (American Society for Stereotactic and Functional Neurosurgery) 2004 Biennial Meeting – Neuromodulation: Defining the Future. Cleveland: Cleveland Clinic Foundation; 2004. Vilela Filho O, RagazzoPC, Silva DJ, Souza JT, Oliveira PM, Ribeiro TMC. Bilateral Globus Pallidus Externus Deep Brain Stimulation (GPe-DBS) for the Treatment of Tourette Sqndrome: an ongoing prospective controlled study (Abstr.). Stereotact Funct Neurosurg 2007;85: 42-3. Vilela Filho O. DBS for Tourette’s syndrome (Abstr.). In Syllabus – CME Conference of the eighth World Congress of the International Neuromodulation Society & 11th Annual Meeting of the North American Neuromodulation Society Acapulco; (Neuromodulation: Technology at the Neural Interface). 2007. p. 21. Vilela Filho O, Ragazzo PC, Silva DJ, Souza JT, Oliveira PM, Ribeiro TM. Bilateral GPe-DBS for Tourette’s Syndrome (Abstr.). Neurotarget 2008;3(1):66. Vilela Filho O. CT-based stereotactic subcaudate tractotomy (SST): technical note (Abstr). Stereotact Funct Neurosurg 2001;76:287-8. Vilela Filho O, Silva DJ, Souza HAO, Cavalcante JES, Souza JT, Ferraz FP, et al. Stereotactic subthalamic nucleus (STN) lesioning for the treatment of Parkinsons’s disease (PD). Stereotact Funct Neurosurg 2001;77: 79-86. Vilela Filho O, Silva DJ. Unilateral subthalamic nucleus lesioning: a safe and effective treatment for Parkinson’s disease. Arq Neuropsiquiatr 2002;60(4):935-48. Vilela Filho O, Silva DJ. STN lesioning for the treatment of Parkinson’s disease: risks and benefits in a long-term follow-up study (Abstr.). Stereotact Funct Neurosurg 2007;85:24. Vilela Filho O, Silva DJ, Souza JT, Ferraz FAP, Cavalcante JES. STN lesioning-induced dyskinesia in patients with Parkinson’s disease: What is behind it? In Abstract Book of the 2003 Quadrennial Meeting of the American Society for Stereotactic and Functional Neurosurgery. New York: New York University Medical School; 2003. p. 198. Vilela Filho O, Silva DJ, Ferraz FP. Evidence for the involvement of the basal ganglia in the genesis of essential tremor (ET) (Abstr.). Stereotact Funct Neurosurg 2001;77:149-50. Vilela Filho O, Ferraz FAP, Barros BA, Barreto PG, Nobrega MDA, Atayde IB, et al. Effects of Unilateral

History of stereotactic and functional neurosurgery in brazil

121.

122.

123.

124.

125.

126.

127.

128. 129.

130.

131.

132.

Posterior Striatotomy on Harmaline-induced Tremor in Rats (Abstr.). Stereotact Funct Neurosurg 2007;85: 29-30. Vilela Filho O, Souza HAO, Cavalcante JES, Dias PCM, Leite MSB. Bio´psia percutaˆnea assistida por tomografia computadorizada de tumores intramedulares (Abstr.). Programa Final do VII Congresso Nacional da Academia Brasileira de Neurocirurgia. Goiaˆnia: Cegraf; 1997. p. 93. Vilela Filho O, Botter W, Jr, Oliveira SB, Teixeira KS. OVF MRI fiducial: a new and long-lasting material for stereotactic MRI (Abstr.). Stereotact Funct Neurosurg 2001;76:191-2. Vilela Filho O, Carneiro Filho O. Gamma probeassisted brain tumor microsurgical resection: a new technique. Arq Neuropsiquiatr 2002;60(4):1042-37. Vilela Filho O, Carneiro Filho O, Arratia JIC, Ragazzo PC, Arruda JB, Costa V, et al. Gamma probe assisted epilepsy surgery: preliminary results of a new technique (Abstr.). Stereotact Funct Neurosurg 2007;85:46. Vilela Filho O, Carneiro R, Jr. MRI-based frameless technique to determine target coordinates (Abstr.). Stereotact Funct Neurosurg 2007;85:62. Pereira LC, Palter VN, Lang AE, Hutchison WD, Lozano AM, Dostrovsky JO. Neuronal activity in the globus pallidus of multiple system atrophy patients. Mov Disord 2004;19(12):1485-92. Saint-Cyr JA, Hoque T, Pereira LC, Dostrovsky JO, Hutchison WD, Mikulis DJ, et al. Localization of clinically effective stimulating electrodes in the human subthalamic nucleus on magnetic resonance imaging. J Neurosurg 2002;97(5):1152-66. Aguiar LR. Biografia do Prof. Dr. Renato de Muggiati (1932–1996). J Bras Neurocirurg 1996;7(3): 56-7. Muggiati R, Ratton JF, Machado S. Resultado sobre 100 pacientes portadores de sı´ndrome de Parkinson tratados cirurgicamente pela talamotomia (Abstr.). In Mattos Pimenta A (Ed). XI Congresso Latino-Americano de Neurocirurgia (Relato´rios Oficiais e Comunicac¸o˜es Livres). Sa˜o Paulo; 1965. p. 272. Francisco AN, Loba˜o CA, Sassaki VS, Garbossa MC, Aguiar LR. Punctate midline myelotomy for the treatment of oncologic visceral pain: analysis of three cases]. Arq Neuropsiquiatr 2006;64(2B):446-50. (Portuguese). Meneses MS, Rocha SB, Kowacs PA, Andrade NO, Santos HL, Narata AP, et al. [Surgical treatment of temporal lobe epilepsy: a series of forty-three cases analysis]. Arq Neuropsiquiatr 2005;63(3A):618-24. (Portuguese). Meneses MS, Rocha SF, Blood MR, Trentin A, Jr, Benites Filho PR, Kowacs PA, et al. [Functional magnetic resonance imaging in the determination of dominant language cerebral area]. Arq Neuropsiquiatr 2004;62(1):61-7. (Portuguese).

16

133. Meneses MS, Follador FR, Arruda WO, Santos HL, Yonesawa D, Hunhevicz SC. [Stereotactic implantation of depth electrodes by magnetic resonance image in epilepsy surgery]. Arq Neuropsiquiatr 1999;57 (3A):628-35. (Portuguese). 134. Meneses MS, Arruda WO, Hunhevicz SC, Ramina R, Pedrozo AA, Tsubouchi MH. Comparison of MRIguided and ventriculography-based stereotactic surgery for Parkinson’s disease. Arq Neuropsiquiatr 1997;55 (3B):547-52. 135. Almeida DB, Poletto PH, Milano JB, Leal AG, Ramina R. Is preoperative occupation related to longterm pain in patients operated for lumbar disc herniation? Arq Neuropsiquiatr 2007;65(3B):758-63. 136. Almeida DB, Hunhevicz S, Bordignon K, Barros E, Mehl AA, Burak Mehl AC, et al. A model for foramen ovale puncture training: Technical note. Acta Neurochir (Wien) 2006;148(8):881-3. 137. Salamoni SD, da Costa JC, Palma MS, Konno K, Nihei K, Azambuja NA, et al. The antiepileptic activity of JSTX-3 is mediated by N-methyl-D-aspartate receptors in human hippocampal neurons. Neuroreport 2005;16 (16):1869-73. 138. Paglioli E, Palmini A, Portuguez M, Paglioli E, Azambuja N, da Costa JC, et al. Seizure and memory outcome following temporal lobe surgery: selective compared with nonselective approaches for hippocampal sclerosis. J Neurosurg 2006;104(1):70-8. 139. Isolan GR, Azambuja N, Paglioli Neto E, Paglioli E. [Hippocampal microsurgical anatomy regarding the selective amygdalohippocampectomy in the Niemeyer’s technique perspective and preoperative method to maximize the corticotomy]. Arq Neuropsiquiatr 2007;65 (4A):1062-9. 140. Ferreira NP, Azambuja NA. [Percutaneous cordotomy]. Arq Neuropsiquiatr 1980;38(1):7-17. 141. Linhares MN, Tasker RR. Microelectrode-guided thalamotomy for Parkinson’s disease. Neurosurgery 2000;46 (2):390-5. 142. Dieckmann G, Veras G. High frequency coagulation of dorsal root entry zone in patients with deafferentation pain. Acta Neurochir 1984; Suppl 33:445–50. 143. Brainer-Lima PT, Rao S, Cukiert A, Yacubian EM, Gronich G, Marino Ju´nior R. Surgical treatment of refractory epilepsy associated with space occupying lesions. Experience and review. Arq Neuropsiquiatr 1996;54(3):384-92. 144. Brainer-Lima PT, Brainer-Lima AM, Azevedo Filho H, Cukiert A. [Partial epilepsy associated to primary brain tumors]. Arq Neuropsiquiatr 2002;60(3-B):797-800. (Portuguese). 145. Brainer-Lima PT, Brainer-Lima AM, Brandt CT, Carneiro GS, Azevedo HC. [Intraoperative mapping of motor areas during brain tumor surgery: electrical stimulation patterns]. Arq Neuropsiquiatr 2005;63 (1):55-60. (Portuguese).

245

246

16

History of stereotactic and functional neurosurgery in brazil

146. Andrade-Souza YM, Zadeh G, Ramani M, Scora D, Tsao MN, Schwartz ML. Testing the radiosurgerybased arteriovenous malformation score and the modified Spetzler-Martin grading system to predict radiosurgical outcome. J Neurosurg 2005;103(4):642-8. 147. Andrade-Souza YM, Schwalb JM, Hamani C, Hoque T, Saint-Cyr J, Lozano AM. Comparison of 2-dimensional magnetic resonance imaging and 3-planar reconstruction methods for targeting the subthalamic nucleus in Parkinson disease. Surg Neurol 2005;63(4):357-62. 148. Andrade-Souza YM, Schwalb JM, Hamani C, Eltahawy H, Hoque T, Saint-Cyr J, et al. Comparison of three methods of targeting the subthalamic nucleus for chronic stimulation in Parkinson’s disease. Neurosurgery 2005;56 (2 Suppl):360-8. 149. Andrade-Souza YM, Zadeh G, Scora D, Tsao MN, Schwartz ML. Radiosurgery for basal ganglia, internal capsule, and thalamus arteriovenous malformation: clinical outcome. Neurosurgery 2005;56(1):56-63. 150. Andrade-Souza YM, Ramani M, Scora D, Tsao MN, TerBrugge K, Schwartz ML. Radiosurgical treatment for rolandic arteriovenous malformations. J Neurosurg 2006;105(5):689-97. 151. Andrade-Souza YM, Ramani M, Scora D, Tsao MN, terBrugge K, Schwartz ML. Embolization before radiosurgery reduces the obliteration rate of arteriovenous malformations. Neurosurgery 2007;60(3):443-51. 152. Steven DA, Andrade-Souza YM, Burneo JG, McLachlan RS, Parrent AG. Insertion of subdural strip electrodes for the investigation of temporal lobe epilepsy. Technical note. J Neurosurg 2007;106(6):1102-6. 153. Andrade-Souza YM, Ramani M, Beachey DJ, Scora D, Tsao MN, Terbrugge K, et al. Liquid embolisation material reduces the delivered radiation dose: a physical experiment. Acta Neurochir (Wien) 2008;150(2):161-4. 154. Holanda MM, Meira UM, Magalha˜es FN, da Silva JA. [Surgical treatment of meralgia paresthetica: case report]. Arq Neuropsiquiatr 2003;61(2A):288-90. (Portuguese). 155. Blond S, Touzet G, Reyns N, Dantas S, Pruvo JP. [Clinical applications of stereotaxic methology]. Ann Fr Anesth Reanim 2002;21(2):162-9. (French). 156. De Salles AA, Katayama Y, Becker DP, Hayes RL. Pain suppression induced by electrical stimulation of the pontine parabrachial region. Experimental study in cats. J Neurosurg 1985;62:397-407. 157. Leichnetz GR, Gonzalo-Ruiz A, De Salles AAF, Hayes RL. The frontal eye field and prefrontal cortex project to the paramedian pontine reticular formation in the cat. Brain Res 1987;416:195-9. 158. Leichnetz GR, Gonzalo-Ruiz A, De Salles AAF, Hayes RL. The origin of brainstem afferents of the paramedian pontine reticular formation in the cat. Brain Res 1987;422:389-97. 159. De Salles AAF, Asfora WT, Abe M, Kjelberg RN. Transposition of target information from the magnetic

160.

161.

162.

163.

164.

165.

166.

167.

168.

169.

170.

171.

172.

resonance and CT-scan images to the conventional x-ray stereotactic space. Appl Neurophysiol 1987; 50:23-32. Anzai Y, Lufkin R, De Salles AAF, Hamilton DR, Farahani K, Black KL. Preliminary experience with MR-guided thermal ablation of brain tumors. AJNR Am J Neuroradiol 1995;16:39-48. De Salles AAF, Frighetto L, Behnke E, Sinha S, Bronstein J, Torres R, et al. Functional neurosurgery in the MRI environment. Minim Invasive Neurosurg 2004;47(5):284-9. Lee WY M, De Salles AAF, Frighetto L, Torres R, Behnke E, Bronstein J. Imaging techniques and electrode fixation methods for deep brain stimulation – Intraoperative MRI 0.2T, 1.5 T and fluoroscopy. Minim Invas Neurosurg 2005;48:1-6. De Salles AAF, Solberg T, Medin P, Vassilev V, Cabatan-Awang C, Selch M. Linear accelerator radiosurgery for trigeminal neuralgia. Radiosurgery 1997;2:173-82. De Salles AAF, Melega WP, Lacan G, Steele LH, Solberg TD. Radiosurgery with a 3 mm collimator in the subthalamic nucleus and substantia nigra of the vervet monkey. J Neurosurg 2001;95:990-7. De Salles AAF, Gorgulho A, Selch M, De Marco J, Agazaryan N. Radiosurgery from the brain to the spine: 20 years experience. Acta Neurochir Suppl 2008;101:163-8. Lacan G, De Salles AA, Gorgulho AA, Krahl SE, Frighetto L, Behnke EJ, et al. Modulation of food intake following deep brain stimulation of the ventromedial hypothalamus in the vervet monkey. Laboratory investigation. J Neurosurg 2008;108(2):336-42. Hamani C, Teno´rio F, Mendez-Otero R, Mello LE. Loss of NADPH diaphorase-positive neurons in the hippocampal formation of chronic pilocarpine-epileptic rats. Hippocampus 1999;9(3):303-13. Hamani C, Mello LE. Status epilepticus induced by pilocarpine and picrotoxin. Epilepsy Res 1997;28 (1):73-82. Hamani C, Luer MS, Dujovny M. Microdialysis in the human brain: review of its applications. Neurol Res 1997;19(3):281-8. Andrade DM, Zumsteg D, Hamani C, Hodaie M, Sarkissian S, Lozano AM, et al. Long-term follow-up of patients with thalamic deep brain stimulation for epilepsy. Neurology 2006;66(10):1571-3. Hamani C, Hodaie M, Chiang J, del Campo M, Andrade DM, Sherman D, et al. Deep brain stimulation of the anterior nucleus of the thalamus: effects of electrical stimulation on pilocarpine-induced seizures and status epilepticus. Epilepsy Res 2008;78(2–3):117-23. Hamani C, McAndrews MP, Cohn M, Oh M, Zumsteg D, Shapiro CM, et al. Memory enhancement induced by hypothalamic/fornix deep brain stimulation. Ann Neurol 2008;63(1):119-23.

History of stereotactic and functional neurosurgery in brazil

173. Weinberger M, Hamani C, Hutchinson WD, Moro E, Lozano AM, Dostrovsky JO. Pedunculopontine nucleus microelectrode recordings in movement disorder patients. Exp Brain Res 2008;188(2):165-74. 174. Toda H, Hamani C, Fawcett AP, Hutchison WD, Lozano AM. The regulation of adult rodent hippocampal neurogenesis by deep brain stimulation. J Neurosurg 2008;108(1):132-8. 175. Hamani C, Saint-Cyr JA, Fraser J, Kaplitt M, Lozano AM. The subthalamic nucleus in the context of movement disorders. Brain 2004;127(Pt 1):4-20. 176. Hamani C, Richter E, Schwalb JM, Lozano AM. Bilateral subthalamic nucleus stimulation for Parkinson’s disease: a systematic review of the clinical literature. Neurosurgery 2005;56(6):1313-21. 177. Hamani C, Neimat J, Lozano AM. Deep brain stimulation for the treatment of Parkinson’s disease. J Neural Transm Suppl 2006;(70):393–9. 178. Hung SW, Hamani C, Lozano AM, Poon YY, Piboolnurak P, Miyasaki JM, et al. Long-term outcome of bilateral pallidal deep brain stimulation for primary cervical dystonia. Neurology 2007;68(6):457-9. 179. Hamani C, Schwalb JM, Rezai AR, Dostrovsky JO, Davis KD, Lozano AM. Deep brain stimulation for chronic neuropathic pain: long-term outcome and the incidence of insertional effect. Pain 2006;125 (1–2):188-96. 180. Richter EO, Davis KD, Hamani C, Hutchison WD, Dostrovsky JO, Lozano AM. Cingulotomy for psychiatric disease: microelectrode guidance, a callosal reference system for documenting lesion location, and clinical results. Neurosurgery 2004;54(3):622-28.

16

181. Machado AG, Baker K, Godwin E, Schuster D, Rezai AR. Electrical stimulation of the cerebellar dentate nucleus enhances recovery of motor function following adult ischemic strokes in adult rats. San Diego; SFN, 2007. 182. Machado AG, Azmi H, Rezai AR. Motor cortex stimulation for chronic benign pain. Clin Neurosurg 2005;54:70-7. 183. Machado A, Ogrin M, Rosenow JM, Henderson JM. A 12-month prospective study of gasserian ganglion stimulation for trigeminal neuropathic pain. Stereotact Funct Neurosurg 2007;85(5):216-24. 184. Machado A, Rezai AR, Kopell BH, Gross RE, Sharan AD, Benabid AL. Deep brain stimulation for Parkinson’s disease: surgical technique and perioperative management. Mov Disord 2006;21 Suppl 14: S247-58. 185. Rezai AR, Machado AG, Deogaonkar M, Azmi H, Kubu C, Boulis NM. Surgery for movement disorders. Neurosurgery 2008;62 Suppl 2:SHC809-39. 186. Kopell BH, Machado AG, Rezai AR. Not your father’s lobotomy: psychiatric surgery revisited. Clin Neurosurg 2005;52:315-30. 187. Machado AG, Malone D, Kopell BH, Greenberg B, Rezai AR. Deep brain stimulation for the treatment of refractory obsessive compulsive disorder: assessment of optimal therapeutic cathode location. San Francisco; Gilbenberg Award. AANS Meeting, 2006. 188. Schiff ND, Giacino JT, Kalmar K, Victor JD, Baker K, Gerber M, et al. Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 2007;448(7153):600-3.

247

10 History of Stereotactic and Functional Neurosurgery in Canada A. G. Parrent

Introduction Functional neurosurgery in its broadest sense includes the surgical treatment of pain, movement disorders, epilepsy and psychiatric conditions. Canada has played a rich and pivotal role in the development of these areas. Wilder Penfield, Herbert Jasper, Ted Rasmussen, Claude Bertrand and Ron Tasker – to mention a few – are names that are familiar to most neurosurgeons who are involved in the practice of functional neurosurgery. This chapter will review some highlights in the development of functional neurosurgery in Canada with an emphasis on stereotactic surgery and epilepsy surgery.

Epilepsy Surgery and the Montreal Neurological Institute In 1928 Edward Archibald, professor of surgery at McGill University, brought Wilder Penfield and William Cone to Montreal, to develop neurosurgery at McGill University. Their clinical work started at the Royal Victoria Hospital and the Montreal General Hospital in Quebec [1]. Penfield [2] had wanted to establish an institute for the scientific study and treatment of neurological disorders and in 1932, the Rockefeller Foundation granted 1.2 million dollars to McGill University for this purpose. This money along with contributions from the city, province and other donors allowed construction of the Montreal Neurological Institute (MNI), which opened #

Springer-Verlag Berlin/Heidelberg 2009

in 1934 as a 50 bed hospital for the investigation and treatment of brain disorders. Penfield’s background included study with Sherrington and Osler at Oxford, Holmes and Greenfield at Queen Square, Cajal and Hortega in Madrid, and Foerster in Breslau. With Foerster he learned the cortical stimulation and excision techniques that he would apply to the treatment of epilepsy. Penfield carried out his first procedure for focal epilepsy at the Royal Victoria Hospital in November 1928, on a young man with posttraumatic epilepsy resulting from a head injury with subdural hematoma and brain contusion after a fall from a horse. At the first operation the motor strip was identified by cortical stimulation and a small adjacent corticectomy was performed. Seizures continued and this man underwent a total of three epilepsy procedures culminating in a wide temporal resection – Penfield’s first temporal lobe resection for epilepsy [3]. Penfield meticulously studied his patients, both clinically and in the operating room and kept detailed records of the results of cortical stimulation. In 1937, Penfield and Boldrey [4] published their results of cortical stimulation mapping in 163 patients marking the first appearance of their motor-sensory homunculus (> Figure 10‐1a, b). Many of our current concepts of cortical localization are based on Penfield’s work [5]. By the early 1950s, Penfield [6] had recognized the unique nature of temporal lobe epilepsy, and introduced the concept of mesial temporal

114

10

History of stereotactic and functional neurosurgery in canada

. Figure 10‐1 (a) Penfield and his surgical team operating on an epilepsy patient who is awake under local anesthesia, in order to identify the epileptic focus by brain mapping. Herbert Jasper, in the glazed gallery, records the electrocorticogram (from Brain vol. 130, figure 10, 2007). (b) The ‘‘homunculus’’ showing areas of cortex related to body movements as evoked by stimulation of the cortex (from Penfield and Boldrey [4])

sclerosis; at that time attributed to herniation of the mesial temporal structures over the edge of the tentorium during difficult childbirth. Penfield and Jasper’s book ‘‘Epilepsy and the functional anatomy of the human brain’’ was published in 1954 and represented a wealth of information on the clinical presentation of epilepsy, observation related to memory, localization of language and surgical aspects of epilepsy treatment [7] (> Figure 10‐2). Penfield was responsible for the recognition of epilepsy as a surgically treatable disease. He utilized electrical stimulation of the cortex in patients undergoing craniotomy under local anesthetic and thereby improved the safety of cortical excisions near eloquent cortex. His technique of subpial dissection resulted in less residual damage and gliosis after corticectomy. This is now a standard technique for epilepsy surgeons. Penfield [1] was Director of the MNI from 1934 to 1960, succeeded by Theodore Rasmussen from 1960 to1972. Rasmussen became Professor

. Figure 10‐2 Penfield and Jasper [7] with manuscript of their book ‘‘Epilepsy and the Functional Anatomy of the Human Brain’’(from Can J Neurol Sci18:540 figure 6)

and Chairman of Neurology and Neurosurgery at the MNI in 1954, coming from the University of Chicago where he was had been Professor of Surgery since 1947 [8].

History of stereotactic and functional neurosurgery in canada

Rasmussen [9–11] added to the MNI’s contributions to the surgical treatment of epilepsy. In his years there he probably performed more operations for epilepsy than any other surgeon of his time. These cases were meticulously followed and his outcome publications report some of the longest follow-ups of epilepsy surgery patients. Rasmussen [12,13] together with Juhn Wada validated the application of the carotid amytal test for lateralization of language function and extended its value by using it for the assessment of memory in candidates for temporal lobe surgery. This is still an important means of testing memory adequacy and reserve in candidates for temporal lobectomy. Rasmussen’s name became attached to the entity of chronic localized encephalitis associated with intractable focal seizures (Rasmussen’s encephalitis); first described by Rasmussen et al. [14] in 1958. Rasmussen and others [15–17] described the condition of cerebral hemisiderosis

10

as a late complication of anatomical hemispherectomy, and introduced functional hemispherectomy as a strategy for preventing it. The MNI continues in its role, not only in the surgical treatment of epilepsy, but also in its role as educator with the training of numerous Canadian and international neurosurgeons, and neurosurgical fellows in these techniques.

Stereotactic and Functional Neurosurgery at the MNI Gilles Bertrand and John Blundell started the functional stereotactic program at the MNI when they performed the first stereotactic pallidotomy in 1958 and the first thalamotomy in 1959 [18]. Gill Bertrand started at the MNI as a resident in 1951 (> Figure 10‐3). John Blundell was invited to join the MNI group in 1957. He was sent to study with Lars Leksell in Sweden and to bring

. Figure 10‐3 (a) Dr. Gilles Bertrand inserting a microelectrode into a patient with Parkinson’s disease. (from Can J Neurol Sci 14:542 figure 8). (b) Gilles Bertrand (left) with Herbert Jasper (right) in 1988. They collaborated from 1964 to 1966 on pioneer studies of microelectrodes recording from basal ganglia neurons in patients undergoing stereotactic surgery for Parkinson’s disease. (from Can J Neurol Sci 26:228 figure 8)

115

116

10

History of stereotactic and functional neurosurgery in canada

. Figure 10‐4 The Jasper and Hunter stereotactic instrument. (from Neurosurgery 2004, 54(5):1246 figure 3)

back a Leksell stereotactic instrument. Prior to this, Drs. Herbert Jasper and John Hunter had constructed a stereotactic frame for human use – but this was never used for clinical purposes. This frame was designed to mount on the operating table with the patient in a sitting position. It was held in place by earplugs, orbital bars and a plate under the upper teeth rather than by skull pins (> Figure 10‐4). They settled on the leukotome of Claude Bertrand for lesion production after studying thermocoagulative lesions in animals and finding great variability of lesion size with identical lesion parameters. At the suggestion of Jasper in 1963 they started using microelectrode recording, and the group adopted a system with a straight microelectrode and one with a curved side arm to record from areas around the central exploring electrode (> Figure 10‐5). This group was one of the first to develop a computer program to assist with operative mapping. It allowed operative stereotactic data to be mapped onto digitized versions of various brain atlases that were expanded or shrunk to match the intercommissural distances of the respective patients [19,20]. Oblique trajectories could be followed interactively through the different

. Figure 10‐5 Leukotome (far left) used for lesion making, curved stimulating electrode (second from left) for performing macrostimulation, three-step electrode (center) used for macrostimulation and evoked potentials, straight and curved tungsten microelectrodes (right). (from Neurosurgery 2004, 54(4):1246 figure 4)

parasagittal planes, and operative physiologic data could be registered to stimulation points for later reference. The leukotome was modeled on the computer screen to allow lesions to be accurately planned and mapped [21,22]. As with all neurosurgical centers, the MNI saw a decline in the number of stereotactic procedures performed for Parkinson’s disease after the introduction of L-dopa. Surgery for other

History of stereotactic and functional neurosurgery in canada

movement disorders patients, mainly essential tremor and dystonia, continued. Abbas Sadikot joined Gilles Bertrand in 1993 and they worked together for a year prior to Bertrand’s retirement from clinical practice. The MNI group continues it work on computerized brain atlases for use in functional neurosurgery. The Leksell stereotactic frame, which was used for their stereotactic procedures, underwent modifications over time. Initial modifications by Bertrand allowed x-rays to be taken through the frame. Later, Andre Olivier made changes to facilitate the insertion of orthogonal electrodes and to make it compatible with angiography and MRI. This became the Olivier–Bertrand–Tipal or OBT frame (OBT frame, Tipal Instruments, Montreal).

10

. Figure 10‐6 Photograph of Claude Bertrand’s pneumotaxic guide with lineated prism to avoid parallax while taking preliminary measurements outside the patient’s head before control x-ray. Also, on the guiding bar, some of the collars could be angulated to allow penetration at an angle or phantom measurements. (from Neurosurgery 2004, 55(3):699 figure 2)

Functional Neurosurgery in Montreal – Hoˆpital Noˆtre-Dame Claude Bertrand was one of the pioneers of stereotactic and functional neurosurgery in Canada. Born in 1917, he obtained his BA (1934), then MD (1940) at the Universite´ de Montre´al. Neurosurgical training at the Montreal Neurological Institute was completed in1946. In 1947 Claude Bertrand established the neurosurgical department at Hoˆpital Noˆtre-Dame in Montreal. Very early in his career he was interested in the treatment of involuntary movement disorders and performed anterior choroidal artery ligation on a number of patients, following Irving Cooper’s lead. In 1953, he carried out the first stereotactic lesioning (pallidotomy) for Parkinson’s disease in Canada. Although stereotactic frames designed by Speigel and Wycis, Riechert and Leksell were available; they usually required general anesthetic for application and Bertrand was looking for something better. He designed a stereotactic device called a pneumotaxic guide that could be applied under local anesthetic, and was used for his procedures [23] (> Figure 10‐6). Unsatisfied

with the inconsistency of lesions produced by cauterization or injection of substances into the brain, he used a leukotome to produce lesions. The original Moniz leukotome with a sharp blade was fairly quickly replaced with a leukotome made with blunt fine piano wire after an intracerebral hemorrhage occurred during one of his procedures [24]. The foramen of Munro was initially used as the anterior landmark for localization but Bertrand was convinced by Guiot to change to the anterior commissure. Influenced by Riechert’s reports [25], Bertrand, like many of his contemporaries moved from the pallidum to the thalamus as the target for Parkinsonian tremor. Bertrand was joined by Sonis N. Martinez in 1956, Jules Hardy in 1962 and Pedro MolinaNegro in 1967. Jules Hardy had completed his neurosurgical training in 1960 and took advantage of a McLaughlin traveling fellowship to work with

117

118

10

History of stereotactic and functional neurosurgery in canada

Gerard Guiot and Denise Albe-Fessard in Paris. There they carried out the some of the first microelectrode recordings in Parkinson’s patients undergoing stereotactic surgery. Following his return to Montreal in 1962, he introduced these techniques to the group and microelectrode recording was used routinely for their functional neurosurgical procedures [24,26] (> Figure 10‐3a). Molina-Negro was the neurophysiologist in the group and involved in the analysis of recordings obtained during stereotactic procedures. He suggested using a proportional measurement system to compensate for variations of individual patient anatomy, and they adopted one in which the AC-PC line was divided into ten equal parts. Using this system, a subthalamic, prelemniscal area target could be delineated with such accuracy that the mere introduction of an electrode was sufficient to arrest tremor [27,28]. One of the major contributions to functional neurosurgery coming from this group was the inception and development of the technique of selective peripheral denervation for the treatment of torticollis [48]. They were unhappy with the results of stereotactic thalamic interventions and wondered whether peripheral denervation could improve the results [18]. They noted that significant though temporary improvement could be produced when active muscles were injected with 1% lidocaine under EMG guidance. Their results of combined thalamotomy and peripheral denervation were reported in 1978 [29]. But they ultimately found that peripheral denervation alone was quite effective for treating torticollis.

The Toronto School The Toronto Neurosurgical program started with Kenneth McKenzie, who broke off from general practice in 1923 to take up a fellowship at the Peter Brent Brigham in Boston. While there he published an article describing sectioning of the anterior cervical spinal nerves along with the

spinal accessory for the treatment of torticollis – a procedure we still call the McKenzie procedure in Canada [30]. He returned to Toronto in 1924 as a surgical resident and went on from there to develop neurosurgery at the Toronto General Hospital. After his retirement in 1952, Dr. Harry Botterell took over the program until 1963 when he left to become Dean of Medicine at Queen’s University in Kingston. The program was then taken over by Dr. Tom Morley. Dr. Ron Tasker (> Figure 10‐7a, b) was a trainee of the Toronto Neurosurgical Program, obtaining his Royal College Fellowship in Neurosurgery in 1959. Tasker spent the following year with Clinton Woolsey at the University of Wisconsin’s Laboratory of Neurophysiology. Woolsey was studying the evolution of the sensorimotor cortex, and carried out cortical mapping in a variety of animals. Tasker developed a great deal of admiration for the ‘simple expressive beauty’ of the figurine charts that were used to represent the results of cortical mapping. Additional time was spent at the National Hospital in Queen Square, London (as was the tradition for Neurosurgical trainees at that time) and in Europe observing Albe-Fessard, Guiot, Riechert, Leksell, Talairach and others. Tasker returned to Toronto September 1961 and started his neurosurgical practice. At that time, functional neurosurgery in Toronto consisted of open cordotomy, the Frazier operation for tic douloureux, open dorsal rhizotomy for pain and the McKenzie operation for torticollis. At that time, stereotactic surgery was used primarily for the treatment of tremor associated with Parkinson’s disease. Pallidotomy was the favored procedure, carried out using ventriculographic guidance and macrostimulation to identify internal capsule. Early on, lesions were made by the inflation of a balloon and instillation of alcohol, or by cryolesioning. Tasker (May 2008, personal communication) rapidly adopted radiofrequency lesioning after its introduction in the early 1960s.

History of stereotactic and functional neurosurgery in canada

10

. Figure 10‐7 (a) Ron Tasker performing stereotactic surgery with one of the earlier Leksell steterotactic frames (b) Tasker (right) with Hirotaro Narabayashi from Japan

Tasker followed Riechert’s lead in moving the tremor target from pallidum to thalamus sometime in the early 1960s [25]. Tasker espoused the philosophy that the stereotactic operating room offered an opportunity to study the physiology of the brain. He established early collaboration with Raimond Emmers, a physiologist at the College of Physicians and Surgeons of Columbia University and later Leslie Organ of the Department of Physiology at the University of Toronto to study the somatosensory pathways of the thalamus and upper midbrain [31]. A computer program was developed to allow mapping of the stimulation responses using Woolsey-type figurines [32]. In 1982, Tasker et al. [33] published this work – ‘‘The Thalamus and Midbrain of Man’’ – which serves as a remarkable body of data and solid reference material for stereotactic and functional neurosurgeons.

Microelectrode mapping was brought into the operating room sometime in the late 1970s. Dostrovsky and Tasker studied the detailed physiology of the motor and sensory thalamus, mentoring numerous masters and PhD students as well as clinical and research fellows. Between 1964 and 1998, 48 such students and fellows were trained by Tasker, many going on to start up stereotactic programs of their own. Tasker took the surgical treatment of movement disorders in Toronto from pallidotomy to thalamotomy then through the reintroduction pallidotomy in the early 1990s. Tasker suggested that one of the great oversights in functional neurosurgery was the failure to recognize that pallidotomy was effective for bradykinesia in Parkinson’s disease. Deep brain stimulation was introduced in the early 1990s following the work of Benabid in Grenoble.

119

120

10

History of stereotactic and functional neurosurgery in canada

Tasker (May 2008, personal communication) was interested in the physiology and treatment of chronic pain. When he started practice pain was categorized as benign or malignant, and there were few operations available for the treatment of pain. Cordotomy was one of the favored procedures, was open and performed bilaterally at T1–2. The other procedure was open mesencephalic tractotomy. One of Tasker’s most significant contributions to pain management was the recognition of the difference between nociceptive pain and deafferentation or neuropathic pain and the breakdown of neuropathic pain into its different components: steady pain, shooting pain and allodynia [34,35]. Tasker has been honored with numerous awards in recognition of his contributions to functional neurosurgery including: the Spiegel & Wycis Medal, awarded by the WSSFN in 1993; the Distinguished Service Award by the ASSFN in 1995; Award for Distinguished Contributions to Pain Research and Management in Canada by the Canadian Pain society in 1997. The Tasker Chair in Functional Neurosurgery was created at the University of Toronto in 1999. In the early 1990s Andres Lozano was recruited to the University of Toronto after completing his neurosurgical training at the MNI. Lozano has expanded the functional neurosurgical program in Toronto and has gone on to be a world leader in stereotactic and functional neurosurgery. Lozano now holds the Tasker Chair at the University of Toronto.

Western Canada Edmonton Howard H. Hepburn started the Neurosurgical program in Edmonton, Alberta in 1920, having completed his medical training at McGill University in 1910. His plans for neurosurgical training in Germany were interrupted by the outbreak of

the first world war. In 1919, he returned to North American and obtained training in neurosurgery at the Mayo Clinic in Rochester. Hepburn was joined in 1945 by Guy Morton who, ultimately assumed leadership of the Neurosurgical Division with Dr. Hepburn’s retirement in 1951. Dr. Thomas Speakman joined the division in 1952. Speakman was trained at the MNI and strongly influenced by Penfield. He started performing stereotactic thalamotomy for Parkinson’s disease in the late 1950s [36] and continued until his sudden death in 1969 at the age of 45.

Saskatchewan Krishna (Kris) Kumar started the functional neurosurgical program in Regina, Saskatchewan in 1961. He came to Canada in 1959 after completing his medical training and surgical residency in Indore, India. He obtained Canadian neurosurgical training under W. D. Stevenson in Halifax and Dr. Morton in Edmonton. In Edmonton, Kumar received training in stereotactic surgery under Dr. Speakman. At the start of his career Dr. Kumar (May 2008, personal communication) was involved in the stereotactic treatment of movement disorders, mainly thalamotomy for Parkinson’s disease. After the introduction of L-dopa and the decline in candidates for movement disorder surgery he concentrated his efforts on the treatment of intractable pain. He was involved in the stereotactic implantation of DBS electrodes in periaqueductal grey (PAG) and sensory thalamus from its start in the late 1960s, and was an advocate of the intravenous pain test for assessing surgical candidacy. This was carried out by injecting small repeated amounts of intravenous morphine to assess the degree of pain relief, and the utilization of naloxone to assess reversibility of the response. Patients responding in a reversible manner to i.v. morphine were considered candidates for PAG stimulation, those not responding were

History of stereotactic and functional neurosurgery in canada

considered better candidates for sensory thalamic stimulation. In general, most patients received simultaneous implantations into both sites followed by percutaneous testing. The most effective electrode was ultimately internalized. The DBS system at the time consisted of a ring electrode activated by a radiofrequencycoupled stimulator (Medtronic). These systems developed slowly; although approved for the treatment of pain in Canada, DBS for pain never obtained FDA approval in the United States. Kumar (May 2008, personal communication) was also involved in spinal stimulation for pain. Starting with the open implantation of intradural and interdural electrodes and through to the epidural systems. The initial percutaneous monopolar electrodes came in straight, sigmashaped and tined varieties. Radiofrequencycoupled systems were eventually supplanted by implanted battery operated systems. Kumar was influential in the development of the fully implantable spinal cord stimulation devices and implantable pumps. Significant contributions to the area of functional neurosurgery include cost-effectiveness studies for spinal cord stimulation and intrathecal drug therapy [37–39], as well as long-term follow-up studies of SCS and DBS for pain [40–42].

British Columbia Frank Turnbull was one of the pioneers of neurosurgery in Canada and the first neurosurgeon in British Columbia. He received his neurosurgical training under K. McKenzie in Toronto, followed by postgraduate work at Queen Square in London, and further work with Foerster in Breslau. He started work at the Vancouver General Hospital in 1933 and devoted special attention to the surgical treatment of intractable pain. Turnbull [43–45] attempted to look at pain syndromes as distinct entities so as to better rationalize management. He published on the pain syndromes associated with

10

pelvic carcinoma and specifically looked at the role of cordotomy in the surgical management of these pain syndromes [45]. The early cordotomies were open procedures, carried out at T1–2. In the mid to late 1960s the switch was made to anterior cervical percutaneous cordotomy. Peter Lehmann joined Frank Turnbull in the late 1940s and started performing thalamotomy for parkinsonian tremor in the late 1950s using the Cooper apparatus and leukotome. Ian Turnbull joined the group in 1966. Ian Turnbull (July 2008, personal communication) obtained his medical training in Vancouver and neurosurgical training in Toronto. While in Toronto he was exposed to Tasker and his work. Residency was followed by a traveling fellowship in Europe gaining exposure to Leksell, Gillingham and others. After his return to Vancouver he rapidly adopted the Todd Wells stereotactic apparatus and used radiofrequency to carry out thalamotomy for tremor disorders. The stereotactic movement disorder program remained active through to his retirement from clinical practice in 1999. In the early 1990s he, like most neurosurgeons switched to pallidotomy for Parkinson’s disease. Ian Turnbull also established and maintained a large pain practice, initially learning the percutaneous cordotomy technique from his father Frank. He favored stimulation of the ventrobasal thalamus for neuropathic pain [46] and reported on combined thalamic or midbrain lesions with cingulumotomy in some patients with nociceptive pain [46].

The Canadian Stereotactic and Functional Neurosurgery Group In 2001 the Canadian Neurosurgical Society formed a Section of Stereotactic and Functional Neurosurgery. The Canadian group is small with only 15 or so neurosurgeons carrying out functional stereotactic procedures in the country. As of 2008, there are active programs in Halifax Nova Scotia,

121

122

10

History of stereotactic and functional neurosurgery in canada

Quebec City and Montreal in Quebec, Toronto and London Ontario, Winnipeg Manitoba, Regina Saskatchewan, Calgary and Edmonton Alberta and Vancouver British Columbia. The relatively small size of the group has been conducive to collaborative work and has resulted in a multicentre study of DBS for cervical dystonia [47]. Other projects are ongoing.

References 1. Feindel W. Development of surgical therapy for epilepsy at the Montreal Neurological Institute. Can J Neurol Sci 1991;18:549-53. 2. Penfield W. No man alone: a neurosurgeon’s life. Boston: Little, Brown & Co; 1977. 3. Foerster O, Penfield W. The structural basis of traumatic epilepsy and results of radical operation. Brain 1930;53 (2):99-119. 4. Penfield W, Boldrey E. Somatic motor and sensory representation in cerebral cortex of man as studied by electrical stimulation. Brain 1937;60(4):389-443. 5. Penfield W, Erickson TC. Epilepsy and cerebral localization. Springfield, IL: Charles C Thomas; 1941. 6. Penfield W, Earle KM, Baldwin M. Incisural sclerosis and temporal lobe seizures produced by hippocampal herniation at birth. Arch Neurol Psychiatry1953;69:17-42. 7. Penfield W, Jasper H. Epilepsy and the functional anatomy of the human brain. Boston: Little, Brown and Company; 1954. 8. Feindel W. Theodore Brown Rasmussen (1910–2002): epilepsy surgeon, scientist and teacher. J Neurosurg 2003;98:631-7. 9. Rasmussen T. Surgical treatment of complex partial seizures: results, lessons and problems. Epilepsia 1983;24 Suppl 1:S65-76. 10. Feindel W, Rasmussen T. Temporal lobectomy with amygdalectomy and minimal hippocampal resection: review of 100 cases. Can J Neurol Sci 1991;18 Suppl 4:603-5. 11. Rasmussen T, Feindel W. Temporal lobectomy: review of 100 cases with major hippocampectomy. Can J Neurol Sci 1991;18 Suppl 4:601-2. 12. Wada J, Rasmussen T. Intracarotid injection of sodium amytal for the lateralization of cerebral speech dominance. Experimental and clinical observations. J Neurosurg 1960;17:266-82. 13. Milner B, Branch C, Rasmussen T. Study of short-term memory after intracarotid injection of sodium amytal. Trans Am Neurol Assoc 1962;87:224-6. 14. Rasmussen T, Olszewski J, Lloyd-Smith D. Focal seizures due to chronic localized encephalitis. Neurology 1958;8: 435-45.

15. Rasmussen T. Postoperative superficial hemosiderosis of the brain, its diagnosis, treatment and prevention. Trans Am Neurol Assoc 1973;98:133-7. 16. Rasmussen T. Hemispherectomy for seizures revisited. Can J Neurol Sci 1983;10:71-8. 17. Falconer MA, Wilson PJ. Complications related to delayed hemorrhage after hemispherectomy. J Neurosurg 1969;30(4):413-26. 18. Bertrand G. Stereotactic surgery at McGill: the early years. Neurosurgery 2004;54:1244-52. 19. Bertrand G, Olivier A, Thompson CJ. Computer display of stereotaxic brain maps and probe tracts. Acta Neurochir Suppl (Wien) 1974;21:235-43. 20. Thompson CJ, Bertrand G. A computer program to aid the neurosurgeon to locate probes used during stereotactic surgery of deep cerebral structures. Comput Programs Biomed 1972;2:265-76. 21. Bertrand G. Computers in functional neurosurgery. In: Rasmussen T, Marino R Jr, editors. Functional neurosurgery. NY: Raven; 1979. 22. Thompson CJ, Bertrand G. A computer program to aid the neurosurgeon to locate probes used during stereotaxic surgery on deep cerebral structures. Comput Programs Biomed 1972;2(4):265-76. 23. Bertrand CM. A pneumotaxic technique for producing localized cerebral lesions, and its use in the treatment of Parkinson’s disease. J Neurosurg 1958;15 (3):251-64. 24. Bertrand CM. Surgery of involuntary movements, particularly stereotactic surgery: reminences. Neurosurgery 2004;55:698-704. 25. Hassler R, Riechert T. lndikationen und lolalisationcmethode der gezielton hirnoperationen. Nervenarzt 1954; 25:441-7. 26. Hardy J. Historical background of stereotactic surgery: reflections on stereotactic surgery and the introduction of microelectrode recording in Montreal. Neurosurgery 2004;54:1508-11. 27. Velasco F, Molina-Negro P, Bertrand C, Hardy J. Further definition of the sub-thalamic target for the arrest of tremor. J Neurosurg 1972;36:184-91. 28. Bertrand C, Hardy J, Molina-Negro P, Martinez SN. Optimum physiological target for the arrest of tremor. In 3rd Symposium on Parkinson’s Disease, Edinburgh, Livingstone, 1969, 251-9. 29. Bertrand C, Molina-Negro P, Martinez SN. Combinedstereotactic and peripheral surgical approach for spasmodic torticollis. Appl Neurophysiol 1978;41: 122-33. 30. McKenzie KG. Intrameningeal division of the spinal accessory and roots of the upper cervical nerves for the treatment of spasmodic torticollis. Surg Gynecol Obstet 1924;39:5-10. 31. Emmers R, Tasker RR. The human somesthetic thalamus. NY: Raven; 1975.

History of stereotactic and functional neurosurgery in canada

32. Tasker RR, Rowe IH, Hawrlyshyn P, Organ LW. Computer mapping of human subcortical sensory pathways during stereotaxis. J Neurol Neurosurg Psychiatry 1975;38 (4):408. 33. Tasker RR, Organ LW, Hawrylyshyn PA. The thalamus and midbrain of man. A physiological atlas using electrical stimulation. Springfield, IL: Charles C Thomas; 1982. 34. Takser RR. Deafferentation. In: Wall PD, Melzak R, editors. Textbook of pain. London: Churchill Livingstone; 1984. p. 639-55. 35. Tasker RR. Management of nociceptive, deafferentation and central pain by surgical intervention. In: Fields HL editor. Pain syndromes in neurology. 2nd ed. London: Butterworths; 1990. p. 143-200. 36. Speakman TJ. Results of thalamotomy for Parkinson’s disease. Can Med Assoc J 1963;89:652-66. 37. Kumar K, Malik S, Demeria D. Treatment of chronic pain with spinal cord stimulation versus alternative therapies: cost-effectiveness analysis. Neurosurgery 2002;51(1): 106-15. 38. Kumar K, Hunter G, Demeria DD. Treatment of chronic pain by using intrathecal drug therapy compared with conventional pain therapies: a cost-effectiveness analysis. J Neurosurg 2002;97(4):803-10. 39. Hornberger J, Kumar K, Verhulst E, Clark MA, Hernandez J. Rechargeable spinal cord stimulation versus nonrechargeable system for patients with failed back surgery syndrome: a cost-consequences analysis. Clin J Pain 2008;24(3):244-52.

10

40. Kumar K, Toth C, Nath RK, Laing P. Epidural spinal cord stimulation for treatment of chronic pain - some predictors of success. A 15-year experience. Surg Neurol 1998;50(2): 110-20. 41. Kumar K, Hunter G, Demeria D. Spinal cord stimulation in treatment of chronic benign pain: challenges in treatment planning and present status, a 22-year experience. Neurosurgery 2006;58(3):481-96. 42. Kumar K, Toth C, Nath RK. Deep brain stimulation for intractable pain: a 15-year experience. Neurosurgery 1997;40(4):736-46. 43. Turnbull F. The nature of pain in the late stages of cancer. Surg Gynecol Obstet 1960;110:665-8. 44. Turnbull F. Intractable pain. Proc R Soc Med 1954;47(2): 155-6. 45. Turnbull F. A basis for decision about cordotomy in cases of pelvic carcinoma. J Neurosurg 1959;16:595-9. 46. Turnbull IM, Shulman R, Woodhurst WB. Thalamic stimulation for neuropathic pain. J Neurosurg 1980;52(4): 486-93. 47. Kiss ZH, Doig-Beyaert K, Eliasziw M, Tsui J, Haffenden A, Suchowersky O. Functional and Stereotactic Section of the Canadian Neurosurgical Society, Canadian Movement Disorders Group. The Canadian multicentre study of deep brain stimulation for cervical dystonia. Brain 2007;130 Pt 11:2879-86. 48. Bertrand C, Molina-Negro P, Martinez SN. Technical aspects of selective peripheral denervation for spasmodic torticollis. Appl Neurophysiol 1982;45:326-39.

123

15 History of Stereotactic Neurosurgery in Italy A. Franzini . V. A. Sironi . G. Broggi

The history of stereotactic neurosurgery in Italy is strictly linked to the development of the mayor European schools of Paris, Stokholm and Freiburg. In the sixties almost any neurosurgical department in Italy had a stereotactic frame dedicated to thalamotomy for Parkinson disease (the Talairach frame, Reichert frame, Guiot frame, Leksell frame and the Cooper frame were the most popular steretactic devices). From this ‘‘pneumoencephalography era’’ we can remember Franco Migliavacca in Milan, Dalle Ore in Verona, Faust D’Andrea in Naple and Elio Tartarini in Genoa who performed thousands of stereotactic operations for Parkinson disease, mental illness, and pain [4]. After the LDopa discovery and its wide therapeutical application, stereotactic surgery seems to have disappeared from Italy except for a few Institutes which still continued to perform stereotactic operations for tremor, pain, dystonia, and epilepsy. So the real first generation of surgeons mainly devoted to functional neurosurgery in Italy in the ‘‘ventriculography era’’ includes Franco Marossero and Paolo Emilio. Maspes in Milan [12,13,14], Victor Aldo Fasano in Turin [7], Gianfranco Rossi [16] and Beniamino Guidetti [11] in Rome. An original stereotactic frame was also developed in Turin and utilized for the treatment of cerebral palsy in adults and children (> Figure 15-1) utilizing alcoholic lesions and later cryothalamotomy. The main interests of the schools of Milan (F. Marossero) and Rome (G. Rossi) were the functional exploration of the brain by acute and chronic implanted electrodes recording deep EEG activity (SEEG) in epilectic patients candidated to tailored resection of the epileptic focus or to #

Springer-Verlag Berlin/Heidelberg 2009

deep radiofrequency lesions of nuclei and tracts involved in the origin and diffusion of the epileptic discharge [13]. Also if this methodology was imported from the Paris School of Talairach and Bancaud, they developed many original observations and contributed to the definition of criteria still utilized worldwide for surgical treatment of epilepsy [12,14]. In those years particularly Gianfranco Rossi had an eminent role in the development of functional and stereotactic neurosurgery in Italy; he therefore deserves a more detailed history. Prof. Rossi worked for 4 years in the field of experimental neurophysiology under the leadership of Prof. Giuseppe Moruzzi and his research interest was centered on the anatomic and functional organization of brainstem reticular formation and sleep physiology. Later when he became chairman of the neurosurgical Department at the Catholic University of Rome his neurophisyological background had a strong influence on clinical practice and research projects and original criteria were proposed to improve the interpretation of electrocerebral epileptic signals. The rationales, indications, and relative efficacy of classic surgical resection approaches including callosotomy, multiple subpial transection, and the so-called lesionectomy were studied [17]. In the same years C. A. Pagni in Milan wrote an universally appreciated book and publications about the surgical treatment of central pain [16]. In that period B. Guidetti in Rome performed operations to treat spasticity (Dentatectomy) and pain (Pulvinotomy) [11]. The main interest of the Turin school was the treatment of cerebral palsy and many thalamotomies have been

194

15

History of stereotactic neurosurgery in italy

. Figure 15-1 Stereotactic thalamotomy performed in the ‘‘pneumoencephalographic era’’ with the Italian frame named FasanoSguazzi. Note the contrast medium (lipiodol)in alcoholic solution injected at the target sites on both sides. (Courtesy of Sergio Zeme M.D., University of Turin, Italy)

performed in dystonic children [7]. The second generation of functional neurosurgeons at the beginning of the ‘‘CT era’’ includes De Divitis in Naples who heralded stereotactic surgery for Gilles de la Tourette syndrome [5]; the senior author (G.B.) who published milestone studies about impedance guided biopsy [1], cell kinetics of deep brain tumors, stereotactic treatment of brain abscesses and pioneered in Europe the treatment of cystic components of craniopharingiomas by intracavitary Bleomycin; founded in Milan the first Italian neurosurgical Department dedicated to functional and stereotactic neurosurgery providing fuel for future development of original treatments such as Deep Brain Stimulation for the treatment of chronic refractory cluster headache and disruptive behaviour. Another master of stereotactic neurosurgery was Franco Frank in Bologna who pioneered surgery of mesencephalic structure to treat cancer pain [8]. Prof. Frank was trained in Freiburg by Mundinger and founded in Bologna the school of functional and stereotactic neurosurgery. His

original approach included nearly all fields of interest of neurosurgery with particular regard to management of brain tumors by intracavitary irradiation and management of pain by stimulation of the periacqueductal gray and thalamus [9]. Massimo Scerrati in Rome and Pierligi De Riu in Sassari [6,18] introduced in Italy the stereotactic brachiterapy of brain tumors. Prof. Scerrati developed the ‘‘Scerrati’s arc’’ to transform the Talairach frame in an isocentric frame [19]. Prof. Mario Meglio in Rome introduced the use of spinal cord stimulation to improve blood flow in peripheral vascular diseases [15]. Belonging to this generation is also Claudio Munari who worked in Paris and Grenoble and founded in Italy the first department entirely dedicated to surgery of epilepsy and functional exploration of the brain. Also in the field of radiosurgery the Italian contribution was significant, particularly due to the contribution of Federico Colombo who applied the linear accelerator to the stereotactic frame and widened considerably the field of application of radiosurgery [3]. Dr. Colombo

History of stereotactic neurosurgery in italy

built up a huge casuistic which includes more than 800 arteriovenous malformations treated by radiosurgery and is one of the larger series of the world. Also in the field of neuroimaging, the Italian contribution was highly represented by Cesare Giorgi who built one the first digitalized stereotactic atlases [10] and developed original equipments in the field of robotics and tridimensional neuronavigation. The ‘‘neuromodulation era’’ heralded at the beginning of the eighties by the senior author [2] belong to the present.

References 1. Broggi G, Franzini A. Value of serial stereotactic biopsies and impedance monitoring in the treatment of deep brain tumours. J Neurol Neurosurg Psychiatry 1981;44(5): 397-401. 2. Broggi G, Franzini A, Giorgi C, Servello D, Spreafico R. Preliminary Results of Specific Thalamic Stimulation for Deafferentation Pain. Acta Neurochir (Wien) Suppl 1984;33:497-500. 3. Colombo F, Benedetti A, Pozza F, Zanardo A, Avanzo RC, Chierego G, Marchetti C. Stereotactic radiosurgery utilizing a linear accelerator. Appl Neurophysiol 1985;48 (1–6):133-45. 4. Dalle Ore G, Da Pian R. Intractable pains and destruction of the latero-ventral nucleus of the thalamus. Presentation of a case of ‘‘phantom limb’’ operated upon with complete success. Minerva Med 1960;29;51:2771-3. 5. de Divitiis E, D’Errico A, Cerillo A. Stereotactic surgery in Gilles de la Tourette syndrome. Acta Neurochir (Wien) 1977;(Suppl 24):73. 6. De Riu PL, Rocca A. Interstitial irradiation therapy of supratentorial gliomas by stereotaxic technique. Long term results. Ital J Neurol Sci 1988;9(3):243-8. 7. Fasano VA, Broggi G, Schiffer D, Urciuoli R. Experimental lesions induced by localized cooling of the brain. Morphologic and histochemical study. Neurochirurgie 1965;11(6):519-28.

15

8. Frank F, Fabrizi AP, Gaist G. Stereotactic mesencephalic tractotomy in the treatment of chronic cancer pain. Acta Neurochir (Wien) 1989;99(1–2):38-40. 9. Frank F, Frank G, Gaist G, Galassi E, Sturiale G, Fabrizi A. Deep brain stimulation in the treatment of chronic pain syndromes. Riv Neurobiol 1982;28 (3–4):309-16. 10. Giorgi C, Garibotto G, Cerchiari U, Broggi G, Franzini A, Koslow M. Neuroanatomical digital image processing in CT-guided stereotactic operations. Appl Neurophysiol 1983;46(1–4):236-9. 11. Guidetti B, Fraioli B. Neurosurgical treatment of spasticity and dyskinesias. Acta Neurochir (Wien) 1977; (Suppl 24):27-39. 12. Marossero F, Ettorre G, Infuso L, Pagni CA. Surgical treatment of non-tumoral epilepsy with stereotaxic methods. Minerva Neurochir 1966;10(4):342-3. 13. Marossero F, Ravagnati L, Sironi VA, Miserocchi G, Franzini A, Ettorre G, Cabrini GP. Late results of stereotactic radiofrequency lesions in epilepsy. Acta Neurochir Suppl (Wien) 1980;30:145-9. 14. Marossero F, Ettorre G, Franzini A, Motti DF. Chronic depth electrodes study of one case of bitemporal epilepsy due to glial tumour. Some physiopathological considerations. Acta Neurochir (Wien) 1978;45(1–2): 123-31. 15. Meglio M, Cioni B, Dal Lago A, De Santis M, Pola P, Serricchio M. Pain control and improvement of peripheral blood flow following epidural spinal cord stimulation: case report. J Neurosurg 1981;54(6):821-3. 16. Pagni CA. Central pain and painful anesthesia. In: Progress in Neurological Surgery vol.8:132-157. (Karger, Basel 1976). 17. Rossi GF. Surgical treatment of partial epilepsy: remarks on the relative role of stereo-EEG and other diagnostic examinations. J Neurosurg Sci 1975;19(1–2):89-94. 18. Scerrati M, Roselli R, Iacoangeli M, Montemaggi P, Cellini N, Falcinelli R, Rossi GF. Comments on brachycurie therapy of cerebral tumours. Acta Neurochir Suppl (Wien) 1989;46:94-6. 19. Scerrati M, Fiorentino A, Fiorentino M, Pola P. Stereotaxic device for polar approaches in orthogonal systems. Technical note. J. Neurosurg 1984;61(6):1146-7.

195

6 History of Stereotactic Neurosurgery in the Nordic Countries B. A. Meyerson . B. Linderoth

In the sixth volume of the classical and comprehensive textbook of neurosurgery by Olivecrona and To¨nnis (1957), Lars Leksell contributed a chapter on ‘‘Targeted Brain Operations’’ (Gezielte Hirnoperationen). In the introduction he refers to the development of his stereotactic instrument – he always preferred to describe his stereotactic frame as a surgical instrument – that followed the pioneering work by Spiegel and Wycis in 1947–1948. The first presentation of Leksell’s sterotactic apparatus dates from 1949 and already in the early 1950s he had gained experience in targeted lesional surgery using electrical current and different types of X-ray beams – radiosurgery. There is no doubt that this makes Leksell, together with a few others, one of the founders of stereotactic surgery. It should also be noted that the principal mode of function and general features of his original instrument have survived in the modern version that is still one of the most commonly used stereotactic systems in the world. That is why the advancement of stereotactic neurosurgery in the Nordic countries is so intimately associated with the name of Lars Leksell and his contributions. Lars Leksell (1907–1986) started his neurosurgical training with Herbert Olivecrona in 1935 at the Serafimer Hospital, one of the oldest hospitals in Sweden founded in 1752. The Olivecrona neurosurgical service enjoyed a solid international reputation and attracted a large number of trainees from all over the world. For a short period Leksell served as a volunteer #

Springer-Verlag Berlin/Heidelberg 2009

medical doctor in Finland when it was attacked by the Soviet Union in November 1939. Later he told that he during that war often speculated on the possibility of extracting bullets from the brain with minimal damage to the surrounding brain tissue using a mechanically guided instrument. In the early 1940s Leksell joined Ragnar Granit, Nobel Laureate 1967, for experimental studies in neurophysiology. In 1945 he presented a PhD dissertation, a monograph on the motor gamma system titled ‘‘The action potential and excitatory effects of the small ventral root fibers to skeletal muscle.’’ This was a major milestone in the understanding of muscle control and has now become part of basic neurophysiology. It should be noted that during these years he, together with Granit and Skoglund, made another major contribution by describing the phenomenon of ephapsis, ‘‘artificial synapses,’’ caused by local pressure on a nerve, as a possible mechanism involved in trigeminal neuralgia. After resuming clinical work, he started work on the development of a stereotactic instrument and in 1947 he visited Wycis in Philadelphia. Leksell described his instrument in a publication in 1949 and this was the first example of a stereotactic system based on the principle of ‘‘center-of-arc’’ in contrast to the Spiegel and Wycis orthogonal, rectangular frame (> Figure 6-1). The use of a movable semi-arc with an electrode carrier implies that the tip of a probe can reach the target regardless of the position of the carrier or the angling of the arc relative to the skull

66

6

History of stereotactic neurosurgery in the nordic countries

. Figure 6-1 The first Leksell stereotactic instrument, based on the ‘‘center-of-arc’’ principle, was described in a publication from 1949

fixation device, i.e., a frame or base plate with bars for bone fixation screws. This construction permits also transphenoidal, straight lateral and suboccipital probe approaches. Leksell was in many respects a perfectionist and for the rest of his life he continued to change and revise the design of virtually every small part of his instrument though the basic semicircular frame was retained. He focused not only on upgrading the function of the instrument but also on its aesthetic appearance. An important feature was that ‘‘the apparatus should be easy to handle and practical in routine clinical work’’ and ‘‘a high degree of exactitude is necessary.’’ An oft-cited quotation is ‘‘Tools used by the surgeon must be adapted to the task and where the human brain is concerned, no tool can be too refined.’’ The first, documented clinical application of Leksell’s stereotactic system was a case of a craniopharyngioma cyst that was punctured and treated with injection of radioactive phosphorus – that patient was probably the first patient in the world to undergo this form of therapy (1948) (> Figure 6-2). Before the advent of modern imaging techniques (CT, MRI), ventriculography was, and in some centers still is, routinely utilized for target

. Figure 6-2 The first practical application of the stereotactic instrument was for puncture of craniopharyngioma cysts

coordinate determination. Already in the late 1940s neuroradiology was a well-developed speciality at the Serafimer Hospital and angiography and pneumoencephalography were routinely practiced. Leksell performed pneumoencephalography, first in the sitting and then in the supine position to visualize the anterior and posterior commissures, respectively. In order to compensate for the divergence of the X-rays, he constructed a diagram of tightly packed concentric circles, approximated to spirals, geometrically related to the divergence and the distance between the X-ray tube and the film, and frame planes, for determining the target coordinates; it has to be admitted, however, that in contrast to Leksell’s other inventions many surgeons found it difficult to understand and use this diagram. Beside the passionate interest in the technical aspects of stereotaxy, Leksell was in the 1950s and 1960s very active in the operation theatre. He performed a large number of pallidotomies, and later also thalamotomies, in Parkinson’s disease and capsulotomies in various forms of

History of stereotactic neurosurgery in the nordic countries

mental disorders (> Figure 6-3). The results of a series of 81 patients subjected to pallidotomy was published in 1960, and 116 patients treated with capsulotomy were reported in 1961. The term and concept of radiosurgery were introduced by Leksell already in 1951 when he reasoned that the ‘‘center-of-arc’’ principle and his first stereotactic instrument were suitable for replacing a probe (needle electrode) by cross-firing intracerebral structures with narrow beams of radiant energy. X-rays were first tried but both gamma rays and ultrasonics were included as alternatives (> Figure 6-4). Initial experiments were performed on cats and then a few patients with pain and chronic psychosis were treated with a 280 kV X-ray tube attached to the arc. Of particular interest is that in 1953 two cases of trigeminal neuralgia were treated and at followup in 1971 they were still free of pain. In 1946 Leksell was appointed head of a neurosurgical unit in Lund in southern Sweden where he became professor in 1958 and remained so until 1960. In those days there were very few neurosurgeons around the world who were active in stereotactic surgery and the international network was very small; it is of interest that the Schaltenbrand and Bailey’s Stereotactic Atlas was partly based on some brain specimens supplied by Leksell. While in Lund, Leksell was apparently able to evade many of his clinical obligations because he was able to initiate a close collaboration with a team of physicists led by Bo¨rje Larsson at the University of Uppsala (north of Stockholm) where a synchrocyclotron was available. They conducted experiments with stereotactic high-energy proton irradiation in goats resulting in a seminal publication in Nature in 1958 (> Figure 6-5). This technique was also applied in a few patients with Parkinson’s disease (pallidotomy), psychiatric disorder (capsulotomy) and pain (mesencephalotomy). Although precisely placed and well-limited lesions could be produced by the focused proton beams, as demonstrated in a few autopsy cases, the synchrocyclotron proved to be too complicated

6

. Figure 6-3 Leksell in the early 1960s with the second generation of his stereotactic frame

. Figure 6-4 Application of the first stereotactic instrument for radiosurgery using cross-firing of 280 kV X-rays. Photo from the early 1950s

for general clinical use. This compelled Leksell to consider other radiation sources and he started designing the 60Co Gamma Unit that was fully integrated with the stereotactic system. The

67

68

6

History of stereotactic neurosurgery in the nordic countries

. Figure 6-5 The first clinical trials with radiosurgery using proton beams from the cyclotron at Uppsala University were performed in the late 1950s

. Figure 6-6 Leksell treating the first case of acoustic neurinoma with the first version of the Gamma Knife in 1968

development of the ‘‘Beam-knife’’ took place after Leksell had been appointed successor to Olivecrona in 1960 and the first unit was inaugurated in 1967 (> Figure 6-6). Later the same year reports of the two first cases, patients with cancer related pain subjected to radiosurgical thalamotomy, were published.

Originally, radiosurgery and the Gamma Unit were developed with the hope that it would offer a bloodless, and less risky, method to be applied principally in functional neurosurgery, for example in thalamotomy for Parkinson’s disease. On the other hand, Leksell had always considered his sterotactic instrument a

History of stereotactic neurosurgery in the nordic countries

surgical tool that should also be utilized in general neurosurgery in order to enhance precision and minimize hazards. This idea had to some extent been realized by the extensive use of stereotactic technique in puncturing cysts and also in performing biopsies in critical regions. However, the Gamma Unit soon proved to be very useful in the treatment of some typical diseases requiring neurosurgery, such as pituitary adenomas, acoustic neurinomas and arteriovenous malformations. This successful application of radiosurgery has indeed revolutionized the management of these conditions but was also met with much skepticism from the neurosurgical community. Albeit the topic of this chapter is the history of stereotaxis, two other examples of Leksell’s exceptionally innovative mind deserve to be mentioned. He was the first to apply ultrasound in neurosurgical diagnosis by the development of echoencephalography as early as 1955. Moreover, his elegantly designed, double action rongeur has become an indispensable tool in the hands of most neurosurgeons.

Leksell’s Disciples Erik-Olof Backlund (1931) started his neurosurgical training in 1960 at the Serafimer Hospital and he soon became a pupil and a close associate of Leksell. At that time neuroradiology could visualize pathological mass processes only indirectly, and therefore stereotactic biopsy was rarely performed, the exceptions being trials to obtain specimens of the cystic wall when performing craniopharyngioma cyst punctures. This became part of Backlund’s doctoral thesis and to facilitate biopsy sampling he constructed a new device consisting of a spiral that could be screwed into the often quite tough craniopharyngioma tissue from which a specimen could then be harvested by using an outer sharp cutting needle as a sleeve punch.

6

This biopsy needle proved to be very useful and is still routinely used. Backlund also contributed other innovative needle instruments for aspiration biopsy, hematoma evacuation, and aqueduct reconstruction. Backlund’s interest in craniopharyngiomas led him to reconsider the choice of radioactive phosphorus for cystic intracavity irradiation and he demonstrated that a colloid 90 Y was more effective. Subsequently, he developed a multimodal treatment program for craniopharyngiomas, and the evacuation of cysts and installation of radioactive substances were in some cases supplemented by radiosurgery of the solid parts (> Figure 6-7). This treatment strategy is still practiced at the Karolinska University Hospital. Another contribution was the application of radiosurgery for capsulotomy in patients with anxiety and OCD; this was first published, with Leksell as co-author, in 1978. As noted by Backlund himself in an autobiographical vignette, the most spectacular phase of his career was the first neurotransplantation of adrenal chromaffin cells in a patient with Parkinson’s disease. This trial was initiated by a group of researchers in basic sciences at the . Figure 6-7 Erik-Olof Backlund (right) and the research engineer Bengt Jernberg (left) preparing a patient for capsulotomy. Note, at that time the head was fixed with a Orthoplast cap. Photo from the mid 1970s

69

70

6

History of stereotactic neurosurgery in the nordic countries

Karolinska Institute and Backlund developed the stereotactic technique for precise depositing of the cellular specimen. Ladislau Steiner (1920) is presumably the most well known of Leksell’s pupils. From 1962 he first trained with Olivecrona who was then still active in spite of retirement. His prime interest was vascular and tumor microsurgery rather than endeavors within the stereotactic and functional field. His first exposure to radiosurgery was when he took part in a major study thalamotomy for cancer-related pain. It then appeared that radiosurgery might be useful for some common neurosurgical diseases also, and together with Leksell he became the first to demonstrate that centrally located arteriovenous malformations, otherwise inaccessible to surgery, could be miraculously obliterated. Steiner, along with Christer Lindquist (1944) who later became one of the leading names in radiosurgery with many important publications, subsequently performed a large number of AVM treatments. Following the first publication many patients from all over the world were referred to him. The AVM experiences triggered a surge of trials on new applications for radiosurgery (acoustic neurinomas, pituitary adenomas, pituitary hormone suppression in Cushing’s disease, pinealomas, meningiomas, and later cerebral metastases). In 1987 Steiner left the Karolinska University Hospital and became professor and director of the Lars Leksell Gamma Knife Center at the University of Virginia. There he created a very active team that has made this center one of the leading ones for radiosurgery. Scientifically also, he has continued to be very active and is co-author of numerous publications covering the entire field of radiosurgery. A few others of Leksell’s disciples who were active in the field of radiosurgery and have made important, more or less independent contributions should be mentioned. Georg Nore´n (1943) was the first to demonstrate, in an extensive and long-lasting study, that the outcome of

radiosurgical treatment of acoustic neurinomas is at least as favorable as that with open surgery performed by the most experienced neurosurgeons. Since 1992, Nore´n has been director of the Gamma Knife Center at Brown University, Providence. Tiit Ra¨hn (1940) became involved in stereotactic techniques and radiosurgery in the late 1960s and he pioneered the management of hormone secreting pituitary adenomas. His career, until retirement, has been entirely devoted to radiosurgery. The senior author of this paper (B.A.M 1933), Meyerson joined Leksell’s team in 1968, shortly after the inauguration of the first Gamma Unit. He soon became involved in ‘‘gammathalamotomy’’ for cancer-related pain and the preliminary results were published in 1969. Because of the relatively unsatisfactory outcome of this form of surgery a project with intracerebral electrical stimulation (deep brain stimulation, DBS) for pain was initiated in 1974, and with electrodes of our own design stimulation was applied simultaneously in several brain targets. This was the beginning of a life-long career in pain research. At an early stage Meyerson was also introduced to surgical treatment of mental disorders and subsequently he performed the great majority of capsulotomies, as well as a large number of interventions for movement disorders, at the Karolinska University Hospital. The second most prominent stereotactic neurosurgeon in the Nordic countries was Lauri Laitinen (1928–2005) and it is notable that he pursued his own career independent of Leksell. He had his basic neurosurgical training in Helsinki and was confronted with stereotactic surgery when working in London, and visiting Gillingham in Edinburgh. He started operating on Parkinsonian patients in 1961 using first the Cooper instrument and later a RiechertMundinger frame. He was, however, dissatisfied with both these instruments and towards the end of the 1960s he had constructed his own system

History of stereotactic neurosurgery in the nordic countries

that was later acquired by many stereotactic centers (> Figure 6-8). This instrument has the Leksell center-of-arc design combined with some features of the Riechert-Mundinger frame. Throughout his career he was very active in clinical practice and performed about 200 thalamotomies annually. During these operations he made extensive trials with impedance monitoring which he found very helpful for differentiating white from grey matter, for example to identify the border between the internal capsule and pallidal tissue. In 1963 Laitinen published his first paper in the field of stereotactic surgery, on the treatment of torticollis. Later he joined with a young neuropsychologist, Juhani Vilkki, and in a series of papers they documented, for the first time, the deterioration of motor, verbal, and visuospatial functions that may occur after thalamotomy. Laitinen was also very interested in pain, and inspired by Gabriel Mazars in Paris, he performed the first trial of implanting a stimulating electrode in a patient with phantom limb pain already in 1968. In 1980 Laitinen moved to Umea˚, a university town in northern Sweden, where he revived stereotactic and functional neurosurgery to such an extent that Umea˚ became a center of excellence. There he developed a device (the

6

‘‘Stereoadapter’’), a light frame that in a reproducible way could be repeatedly attached to the skull during CT and MRI examinations and then utilized for coordinate determination together with the original frame. In 1984 he, along with Marwan Hariz (who later became his successor) and Tommy Bergenheim, began to test Leksell’s old and almost forgotten version of pallidotomy from the early 1950s. For many of the younger neurosurgeons this endeavor is directly associated with the name of Laitinen. It should be recalled that with the advent of L-dopa in the early 1970s the use of surgery for movement disorders, in particular for Parkinson’s disease, was reduced to just a few cases each year even in the major centers. The first presentation in 1992 of the favorable outcome of Laitinen’s pallidotomy cases resulted in a dramatic change in attitude toward surgery among the neurologists. A contributing, important factor was that this type of intervention had proven to be effective for L-dopa induced hyperkinesias also, which by that time had become a major problem. No doubt, the acceptance of pallidal surgery following Laitinen’s reports paved the way for the ensuing development of stimulation of central brain areas (DBS) as a novel mode of therapy for Parkinson’s disease.

. Figure 6-8 Lauri Laitinen standing by a case displaying his own frame and stereoadapter. Photo from 2003

71

72

6

History of stereotactic neurosurgery in the nordic countries

During the 1960–1970s stereotactic surgery was practised occasionally in a few other neurosurgical units in the Nordic countries but these activities cannot be regarded as pioneering or innovative. One exception was the contributions made by Kjeld Vaernet (1920–2006) in Copenhagen who in 1974 reported on a trial with ‘‘stereotactic stimulation and electrocoagulaton of the lateral hypothamus’’ in five patients with gross obesity. He also performed many stereotactic surgeries for epilepsy and mental disorders. Even though the contributions of Leksell are exceptional and outstanding, the importance of the achievements of his disciples and of Laitinen in making the Nordic countries strong in stereotactic open neurosurgery and radiosurgery should not be underestimated.

Selected Bibliography 1. Backlund EO, Granberg PO, Hamberger B, Knutsson E, Martensson A, Sedvall G, Seiger A, Olson L. Transplantation of adrenal medullary tissue to striatum in parkinsonism: first clinical trials. J Neurosurg 1985;62: 169-73. 2. Backlund EO. Reflections: a historical vignette. Neurosurgery 2004;54:734-41. 3. Backlund EO, Johansson L, Sarby B. Studies on craniopharyngiomas. II. Treatment by stereotaxis and radiosurgery. Acta Chir Scand 1972;138:749-59. 4. Bingley T, Leksell L, Meyerson BA, Rylander G. Stereotaxic anterior capsulotomy in anxiety and obsessivecompulsive states. Third World Congress of Psychosurgery, Cambridge: University of Cambridge Press; 1972. p. 159-64. 5. Boe¨thius J, Lindblom U, Meyerson BA, Wide´n L. Effects of multifocal brain stimulation on pain and somatosensory functions. In: Zotterman Y, editor. Sensory functions of the skin in primates with special reference to man. New York: Pergamon Press; 1976. p. 531-48. 6. Hirsch A, Nore´n G, Anderson H. Audiologic findings after stereotactic radiosurgery in nine cases of acoustic neurinomas. Acta Otolaryngol 1979;88:155-60. 7. Laitinen LV. A new stereoencephalotome. Zentralbl Neurochir 1971; 32: 67-73. 8. Laitinen LV, Bergenheim AT, Hariz MI: Leksell’s posteroventral pallidotomy in the treatment of Parkinson’s disease. J Neurosurg 1992;76:53-61.

9. Laitinen LV. Personal memories of the history of stereotactic neurosurgery. Neurosurgery 2004;55:1420-8. 10. Larsson B, Leksell L, Rexed B, Sourander P, Mair W, Andersson B. The high-energy proton beam as a neurosurgical tool. Nature 1958;182(4644):1222-3. 11. Lindquist C, Kihlstro¨m L. Department of Neurosurgery, Karolinska Institute: 60 years. Neurosurgery 1996;39: 1016-21. 12. Leksell L. The action potential and excitatory effects of the small ventral root fibres to skeletal muscle. Acta Physiol Scand 1945;10 Suppl 31:1-79. 13. Leksell L. A stereotaxic apparatus for intracerebral surgery. Acta Chir Scand 1949;99:229-33. 14. Leksell L. The stereotaxic method and radiosurgery of the brain. Acta Chir Scand 1951;102:316-9. 15. Leksell L, Lide´n K. A therapeutic trial with radioactive isotopes in cystic brain tumor. In: Radioisotope techniques. Proceedings of the isotope techniques conference, Vol 1. Oxford: H.M. Stationary Office 1953; 1951. p. 76-8. 16. Leksell L. Gezielte Hirnoperationen. In: Olivecrona H and To¨nnis W, editors. Handbuch der Neurochirurgie, Vol 6., Berlin: Springer-Verlag; 1957. p. 178-99. 17. Leksell L. Some principles and technical aspects of stereotaxic surgery. In: Knighton RS and Dumke PR, editors. Pain. Boston: Little, Brown and Company; 1966. p. 493-502. 18. Leksell L. Cerebral radiosurgery. I. Gammathalamotomy in two cases of intractable pain. Acta Chir Scand 1968;134:585-95. 19. Leksell L, Backlund EO, Johansson L. Treatment of craniopharyngiomas. Acta Chir Scand 1967;133:345-50. 20. Leksell L. A note on the treatment of acoustic tumours. Acta Chir Scand 1971;137:763-5. 21. Leksell L. Sterotaxic radiosurgery in trigeminal neuralgia. Acta Chir Scand 1971;137:311-4. 22. LeksellL, Backlund EO. [Radiosurgical capsulotomy – a closed surgical method for psychiatric surgery] Lakartidningen 1978;75:546-7 (Swedish). 23. Nore´n G, Arndt J, Hindmarsh T. Stereotactic radiosurgery in cases of acoustic neurinoma: further experiences. Neurosurgery 1983;13:12-22. 24. Quaade F, Vaernet K, Larsson S. Stereotaxic stimulation and electrocoagulation of the lateral hypothalamus in obese humans. Acta Neurochir (Wien) 1974;30:111-7. 25. Ra¨hn T, Thore´n M, Hall K, Backlund EO. Stereotactic radiosurgery in Cushing’s syndrome: acute radiation effects. Surg Neurol 1980;14:85-92. 26. Steiner L, Leksell L, Greitz T, Forster DMC, Backlund EO. Stereotaxic radiosurgery for cerebral arteriovenous malformations: report of a case. Acta Chir Scand 1972; 138:459-64. 27. Svennilson E, Torvik A, Lowe R, Leksell L. Treatment of parkinsonism by stereotatic thermolesions in the pallidal region. A clinical evaluation of 81 cases. Acta Psychiatr Scand 1960; 35: 358-77.

History of Stereotactic Surgery

1 History of Stereotactic Surgery P. L. Gildenberg . J. K. Krauss

Preface In order to define when stereotactic surgery started, it is first necessary to define what stereotactic surgery is [1]. ‘‘Stereotaxic’’ surgery began in 1908, when Sir Victor Horsley and Robert Clarke [2] introduced their new apparatus to allow them to insert a probe, blade, or needle under accurate control into a subcortical structure of a monkey or other experimental animal. They specified the use of a Cartesian coordinate system [3] that makes it possible to define a point in space by specifying three coordinates, anterior-posterior (AP), lateral and vertical, and that Cartesian system remains the hallmark of stereotactic systems. Sir Victor Horsley was both a neurosurgeon and neurophysiologist, and is generally recognized as the father of human functional neurosurgery. He had collaborated with Robert Clarke, a mathematician and also a surgeon, and recruited him to help him design their device. The design and mathematics of the instrument was mainly Clarke’s, and the details of how it might be used were Horsley’s [4]. Their initial report of an experiment conducted with this apparatus concerned making electrolytic lesions in the dentate nucleus of the cerebellum of the monkey to study its structure and functions [2] (> Figure 1-1). The 1908 article that introduces stereotaxic surgery is a magnificent illustration of a literary scientific journal article, and the original should be read by anyone with an appreciation of the history of medical literature. The article is divided into four parts. One part describes the first animal stereotaxic apparatus, which has remained a model for most such devices, both for animals and patients, over this past century (> Figure 1-1). #

Springer-Verlag Berlin/Heidelberg 2009

In order to define a target point, they used Cartesian coordinates, that is, defining a point in space by its relationship to three planes, each at right angles to the other two, and all meeting at a common point as shown in > Figure 1-2. A location can be defined by three coordinates, each of which tells the relationship (in this case in millimeters) to one of the three planes – x mm anterior or posterior to the coronal plane, y mm lateral to the midsagittal plane, and z mm above or below the horizontal plane. For that to have relevance to the structures within the animal brain, the three planes must be registered, or accurately aligned, to the position of the head of the experimental animal. This was accomplished by relating the three planes to the same parts of the device that held the head securely – [6] a horizontal plane (similar to the Frankfort plane used in anthropology [6]) that passed through both ear plugs and a tab that held the left inferior orbital rim (or both if there is no asymmetry) from which to define the vertical coordinate – [7] a mid-sagittal plane that passes through the mid-point between the ear plugs at right angles to the horizontal plane to define the left or right lateral coordinate – and [8] a coronal plane that passes through the ear plugs and is perpendicular to the other two planes to define the AP coordinate. The second part of the Horsley-Clarke paper is a technique for making a stereotactic atlas registered to this same Cartesian system, in which the stereotaxic coordinates of a particular structure could be found. The third part was an excellent treatise about making direct current electrolytic lesions. The fourth and least remembered part was the experiment itself. Clarke suggested to Horsley that the technique might be useful in humans, and even

4

1

History of stereotactic surgery

. Figure 1-1 The original Horsley-Clarke apparatus [2]

. Figure 1-2 The concept of Cartesian planes to measure coordinates aligned with third ventricle

patented the idea of a human stereotactic apparatus, still based on using the boney landmarks to establish the landmarks from which Cartesian coordinates might be determined [9,10]. The

pair separated because of other disagreements, so neither pursued the idea of a human stereotactic any further [11]. In 1918, however, Mussen, an engineer who had been involved in making the Horsley-Clarke apparatus designed a similar device for use with the human skull [12]. There is no evidence that he persuaded any of his neurosurgical colleagues to use it, so he eventually wrapped it in newspaper and stored it in a box in his attic. When his family discovered the box almost 60 years after the Mussen frame had been made, they could determine when it had been stored by the date on the newspaper wrapping. It is perhaps best that it was not used, because it has since become known that the relationship between the boney landmarks on the human skull and the cerebral structures within are so variable that accurate targeting would not have been possible. It took most of the 40 years after the 1908 report that concepts of human physiology became well enough known to have determined the appropriate intracerebral subcortical targets. Let us digress for a moment to confront two other issues involving [6] devices prior to Horsley and Clarke and [7] the spelling of ‘‘stereotaxic’’ versus ‘‘stereotactic.’’ There were reports of a variety of devices to guide a probe into the brain or spinal cord prior to 1908, with consequent claims of a variety of ‘‘first’’ stereotactic devices. We are unaware of any prior system that used a Cartesian coordinate system. Most used overlying landmarks to approximate the location of various structures. Probably the first such system was that presented by Dittmar [13] in 1873, in which he used a guided probe to insert a blade into the medulla oblongata of the rat to perform physiological studies. From the Russian perspective, the beginnings of human stereotactic surgery are ascribed to Zernov [14], who in 1889 described an ‘‘encephalometer’’ that helped localize cortical areas, and Altukhov [15] who used it clinically 2 years later. This was not Cartesian in principle and did

History of stereotactic surgery

not address the localization of deep subcortical structures. In regard to the spelling of the technology addressed throughout this book, there is a logic to it. Horsley and Clarke called their technique ‘‘stereotaxic,’’ from the Greek ‘‘stereos,’’ threedimensional, and ‘‘taxus,’’ an arrangement, as in taxonomy. In a meeting in 1973 when it was decided to change the name of the ‘‘International Society for Research in Stereoencephalotomy’’ (meaning three-dimensional study of the encephalon or brain), it became necessary to agree on a spelling. Since the advent of human stereotactic surgery, some authors, mainly in Europe, used the spelling ‘‘stereotactic,’’ rather than ‘‘stereotaxic,’’ although the origins of that spelling have been lost. A vote was taken as to whether the newly named society would be spelled ‘‘stereotaxic’’ (‘‘three-dimensional’’ and ‘‘arrangement,’’ both from Greek), or ‘‘stereotactic’’ (a mongrel word meaning ‘‘three-dimensional’’ from Greek and ‘‘tactus’’ from Latin ‘‘to touch’’). It was felt that the object of the surgery was actually to touch the desired structure with a probe or electrode, so by vote the decision was made to spell the society ‘‘Stereotactic.’’ In a prescient moment, the decision was also made to call the societies which followed the International Society for Research in Stereoencephalotomy, the World Society for Stereotactic and Functional Neurosurgery, the American Society for Stereotactic and Functional Neurosurgery, and the European Society for Stereotactic and Functional Neurosurgery, ‘‘stereotactic’’ to denote the manner of localization (how you get to the target) and ‘‘functional,’’ meaning to change the function of the brain (what you do after you get there) [16]. The word ‘‘stereotaxis’’ refers to both animal and human procedures. The convention of referring to human surgery as ‘‘stereotactic’’ and animal surgery as ‘‘stereotaxic’’ has been generally adopted and will be maintained throughout this review. History is not a straight line. Different topics that relate to stereotactic surgery developed at

1

the same time, but often with different chronology. More often, advances in other fields became incorporated into stereotactic technique at various stages of development while other things were happening within stereotaxis itself. Consequently history cannot be presented as a continuum. We will digress as occasion demands, take side trips if they appear to be interesting, and double back on the calendar as we switch from one topic to another. The major topics will have separate titles, and subtopics will be announced in bold type, which signifies a change in gears and often a change in direction. After introducing the technology, we will take movement disorder surgery up to 1968, where we can pause that story, discuss other indications for functional neurosurgery, and then come back to the reawakening of stereotactic movement disorder surgery in 1992.

Birth of Human Stereotactic Surgery The problem of establishing accurate intracerebral landmarks from which specific brain structures could be measured and building a device to insert an electrode accurately to a chosen anatomical structure is credited to Ernest A. Spiegel and Henry T. Wycis (> Figure 1-3). Spiegel was a neurologist and neurophysiologist who fled the Nazis in Vienna and emigrated to Temple Medical School in Philadelphia as Professor of Experimental Neurology [17]. (His wife, Mona Spiegel-Adolph, was simultaneously recruited as Professor of Colloid Chemistry). Wycis began to work in Spiegel’s laboratory when he was a medical student, and their collaboration developed throughout his neurosurgical residency and appointment to the faculty [18]. In 1947, they reported on the first use of a human stereotactic apparatus they had designed (still spelled ‘‘stereotaxic’’ at that time) [5].

5

6

1

History of stereotactic surgery

. Figure 1-3 Spiegel and Wycis with their Model V apparatus [19]

The time was right for development of human stereotactic surgery (> Figures 1-4 and > 1-5). The motivation was there: Prefrontal lobotomy had been popular and was indicated in many cases, prior to the development of psychotropic medication, but then it became abused by some [20]. One main motivation to develop stereotactic surgery was to provide a controlled lobotomy effect with less risk of unintended neurological deficit. Once stereotaxis was available, however, the first patients were those with movement disorders, and its use in psychosurgery was not reported for several years. The technology had just been developed: One key to this field was the first introduction of X-ray equipment into the operating room with rapid film development. The key to human stereotactic surgery is to identify landmarks within the brain by X-ray or by other imaging and calculating where a target lay in relation to those landmarks. Ventriculogram X-rays could be taken to visualize internal cerebral landmarks about the third ventricle, from which measurement could be made to localize any cerebral

. Figure 1-4 The original Spiegel-Wycis stereotactic apparatus [5]

. Figure 1-5 Spiegel and Wycis in the operating room. Note the Faraday cage to shield electrical noise so recording could be done

History of stereotactic surgery

structure [5]. This made it possible to use intracerebral landmarks, usually around the third ventricle, from which to measure the three coordinates, each of which was based on one of the three Cartesian planes, hence the AP, lateral, and vertical coordinate (> Figure 1-2). The location of a specific structure required reference to a human stereotactic atlas, which they published soon after stereoencephalotomy was introduced [21] (> Figure 1-6). The science was there: The field of neurophysiology had advanced to the point where targets could be selected on a rational basis. An appreciation of the extra-pyramidal system was emerging, and it was recognized that many movement disorders involved those circuits. Surgical feasibility was demonstrated by Meyers [22] (> Figure 1-7) – series of 38 patients reported in 1942 (> Figure 1-8). There were also attempts to interrupt pathways in the brain for management of pain. Many of these techniques involved surgical interruption of conveniently superficial pathways and are still in use [24–26]. There was a good concept

. Figure 1-6 The orientation of slices in a stereotactic atlas

1

of the primary pain pathway as it ascends through the brainstem, and the concept that the limbic system participated in pain perception was becoming well developed [27,28]. The engineering was there: Spiegel and Wycis [21] called their new technique ‘‘stereoencephalotomy,’’ a three-dimensional system based on brain measurements. The device was essentially a Horsley-Clarke apparatus suspended over the patient’s head, secured to a ring held by a plaster cap made for each patient individually (> Figure 1-3). The ring was aligned with the horizontal plane by ear plugs so that AP and lateral X-rays could be taken accurately and repeatedly. A microdrive supported by the ring was mounted above the patient’s head to hold the electrode and advance it either vertically or obliquely into the target within the brain. They originally selected the anterior commissure and the pineal gland as the two basic landmarks, and produced a stereotactic atlas based on measurements between those structures and the desired target [21]. The use of the anterior and posterior commissure was made a decade later

7

8

1

History of stereotactic surgery

. Figure 1-7 Russel Meyers, 1904–1999 [23]

. Figure 1-8 Meyers’ open surgical approach to the basal ganglia [23]

by Talairach and his associates [29], which, with some variations, were adopted by most stereotactic neurosurgeons. Originally, X-ray visualization of the landmarks about the ventricle required a pneumoencephalogram [21,30], which made it mandatory that the stereotactic apparatus could be accurately reapplied, which was the protocol when

I (plg) first started working as a medical student with Spiegel and Wycis [18,31] in 1956. Patients had the device attached on Tuesday, pneumoencephalogram performed, and measurement made. The apparatus was removed, because the patient by that time was too sick to have a procedure performed under local anesthesia. The patient was returned to the operating room 2 days later to replace the head ring and for the actual surgery. When positive contrast agents became available, it became possible to do the surgery at a single session [18]. A philosophy that was begun with the first Spiegel-Wycis procedure and maintained through the years by most stereotacticians is that each time an electrode is inserted into the brain it produces a unique opportunity to study human neurophysiology, so each procedure included both physiological confirmation of the electrode position and neurophysiologic studies [32]. Not only did this provide a confirmation of the intended target, but led to advances in our understanding of the human brain and the diseases being treated. Originally, the lesions were made with alcohol injection, which theoretically was more likely to affect the neurons in the intended nucleus while sparing the fibres en passage. The spread of the alcohol was unpredictable, however, so soon lesions were made with the same electrolytic direct current that Horsley and Clarke had reported almost half a century before [2]. However, that carried the risk of a sudden sharp stimulation if the current varied. Other techniques were soon developed, such as oil-procaine or oil-procaine-wax injection [33,34], alcohol injection, sometimes with a balloon cannula or coagulating substance [35,36], mechanical damage with a leukotome [37], and later radiofrequency [38] and cryoprobe methods [39]. The original report by Spiegel and Wycis [5] ended by enumerating a list of potential indications for stereotactic surgery. It is almost certain that they had used this new procedure for all those indications prior to their first publication.

History of stereotactic surgery

The interest was there: The first decade after human stereotactic surgery was introduced was particularly productive. There was a stream of neurosurgeons from throughout the world visiting Spiegel and Wycis’ service at Temple Medical School in Philadelphia, learning this new technique and returning home to enter this new field. It was necessary for each to design and manufacture his own stereotactic frame, since there were none commercially available. A variety of apparatus was rapidly introduced, including several advanced designs by Spiegel and Wycis, so that they did most of their work with the Model V [19]. All told, during the 1950’s, at least 40 other stereotactic apparatus were designed along the three basic types. The Spiegel-Wycis system required translational adjustments, as did the Horsley-Clarke apparatus, in that the position of the electrode was changed by sliding the electrode carrier anterior-posterior and laterally along a base plate, to adjust to the proper coordinates, the vertical adjustment was made by a microdrive system holding the electrode. The predetermined trajectory might require two separate angular adjustments. Other devices rapidly followed [40]. Lars Leksell [41] returned home to Sweden after a trip to Philadelphia and designed the first arc centered device in 1948. The three coordinates indicated the center of a semicircular arc along which an electrode carrier moved, so it always pointed to the isocenter at which the target lay. Since the target always lies in the center of the arc, insertion along any angle would bring the probe to the target. The following year, Talairach [42] in Paris designed a system which involved the insertion of electrodes through a fixed grid system, which in turn invited an elaboration of the cerebral circulation. In Germany, Riechert and Wolff [43] reported in 1951 their translational system, which included the first phantom base to verify the settings mechanically.

1

Bailey and Stein [44] exhibited a burr hole mounted apparatus in the United States that same year. It was essentially a pointing device mounted on a ball and socket joint. The electrode was aligned with the intended trajectory drawn on both the AP and lateral films, resulting in an angular adjustment pointing at the target. Parallax was corrected by repeatedly adjusting to repeated films as the electrode was further advanced, a system of successive approximations. Special note must be made of the development of Narabayashi’s [45,46] system in Japan. He had been cut off from the western literature at the end of World War II, but independently developed an apparatus under difficult circumstances [47]. After finding out that his system was not unique, he conceded that Spiegel and Wycis had preceded his contribution. In the first decade after stereotactic surgery was born, a number of centers were developed throughout the world. Leksell in Sweden [41]. Talairach and associates [48] and Guiot and colleagues [49] in France. Riechert and Mundinger [50] in Germany. Gillingham [51] in Great Britain, Laitinen and Toivakka [52] in Finland, Rossi [53] in Italy, Bertand and colleagues [54] in Canada, Velasco Suarez and Escobedo [55] in Mexico, Obrador [37] in Spain, and Bechtereva and colleagues [56] and Kandel [57] in Russia, among others. Each investigator in turn added his own embellishments and indications, and the field grew rapidly. Within 20 years, stereotactic surgery was practiced throughout the world [58,59]. It is estimated that by 1965 more than 25,000 stereotactic treatments had been done worldwide [60], and 37,000 patients had been treated by 1969 [61]. The need for communication among this handful of pioneers required meeting together, and the stereotactic societies were born. The first meeting of the International Society for Research in Stereoencephalotomy (which became the World Society for Stereotactic and Functional Neurosurgery in 1973) was held in Philadelphia

9

10

1

History of stereotactic surgery

in 1966, 20 years after the first human stereotactic procedure. The emphasis was on instrumentation, since there were still few commercially available apparatus. Everyone was invited to bring their stereotactic apparatus, or at least the portable portion. Over 40 systems were laid out on the benches in the chemistry laboratory and demonstrated. The second meeting was held in Atlantic City the following year and the emphasis was on the growing number of indications for stereotactic surgery. During the 1960’s, the Todd-Wells stereotactic apparatus became the most popular in the United States, and the Leksell and RiechertMundinger systems in Europe [62,63]. There was little further modification of apparatus during the next decade, when the emphasis shifted to indications and results. The indications were there: There are four fields in which stereotactic functional neurosurgery has found a place, and all four were established during the first decade after stereotactic surgery was introduced: movement disorders, pain, epilepsy and psychiatric abnormalities. The most cited is the use of stereotactic techniques for treatment of movement disorders. Historically stereotactic surgery was developed to offer a more refined way of doing psychosurgery, without the gross inaccuracies and complications of pre-frontal lobotomy. Treatment of pain was addressed very early in the history of this new technique. Although there were early attempts at treating epilepsy with stereotactic surgery, they were less successful and became more important later, after imaging and invasive monitoring were introduced.

Movement Disorders – the Early Years Although the origin of functional neurosurgery was motivated by a need to improve psychosurgery, the first patient had a motor disorder (Huntington’s chorea).

There was growing understanding that interruption of the extrapyramidal system might benefit patients with movement disorders, particularly Parkinson’s disease, but pre-existing surgical techniques had unacceptable morbidity and mortality. The evolution of surgery for Parkinson’s disease deserves mention. Before the introduction of stereotactic techniques, the most common surgery for movement disorders involved resection of the motor or pre-motor cortex, since it was proposed as early as 1932 by Bucy and Buchanan [64] that it was necessary to interrupt the pyramidal system to obtain relief of athetosis. Shortly after that, Bucy [65,66] also claimed relief of tremor after interruption of the pyramidal system, even though the procedure was fraught with severe post-operative deficits. In 1933, Putnam [67] interrupted the proprioceptive input by posterolateral cordotomy in an attempt to lessen tremor and rigidity with less risk. Walker [68], on the other hand, who had reported mesencephalotomy for pain in 1942, attacked the extrapyramidal pathways at that same mesencephalic level in 1949 by incising the peduncle [68,69], which was reported also about that same time by Guiot and Pecker [70] (and will have some historical importance later in this story). It was the often under-appreciated Russel Meyers [22,23] at the University of Iowa who provided the surgical observations that led to the definition of targets that would soon thereafter become targets for stereotactic surgery. Up to the early 1940s it was thought that a lesion involving the extrapyramidal system would result in irreversible coma, a conclusion that was based on Dandy’s observations that frontal lobe stroke involving the basal ganglia was invariably lethal [71,72]; because Dandy has so stated it was not challenged. Meyers [73] defied that convention and reported in 1939 benefit in a single patient with Parkinson’s disease from surgical extirpation of the head of the caudate nucleus. He was encouraged to investigate further, and he devised

History of stereotactic surgery

intricate non-stereotactic interhemispheric and transventricular approaches to interrupt the ansa lenticularis at the base of the globus pallidus, which he reported in 1942. Since there were no drugs effective against the manifestations of Parkinson’s disease, adventurous surgery was often indicated, but even Meyers cautioned against its general use, as he reported a mortality rate of 15.7%. In contrast, within a decade, after stereotactic surgery was introduced, Spiegel and Wycis [74] reported operative mortality of 2% to attain an even more accurate interruption of the extrapyramidal system. Riechert and Mundinger [75] soon after reported a mortality rate less than 1%, where it remains today. Although the first reported stereotactic case involved pallidotomy for Huntington’s chorea [5], Spiegel and Wycis were initially reluctant to lesion that structure for Parkinson’s disease for fear that the hypokinesia that is seen after experimental pallidotomy might make Parkinson akinesia worse. However, Hassler and Riechert [76] reported in 1954 that they had successfully treated Parkinson’s disease as early as in 1952 by ventrolateral thalamotomy. This encouraged Speigel and Wycis [77] to lesion the ansa lenticularis fibers as they emerged from the pallidum, which they termed pallido-ansotomy. At about the same time, Narabayashi and Okuma [33] made a lesion within the pallidum with procaine-oil injection. The first patient who had stereotactic surgery in 1947 had two lesions made by alcohol injection, one in the globus pallidus and one in the dorsomedial thalamus [5]. The reasons for using two targets were [6] to interrupt the extrapyramidal circuit in the pallidum and [7] to lessen the emotional tone of the patient by interrupting the thalamic projections to the frontal lobe, since it was recognized that tension made the chorea worse. Although the patient had only moderate but temporary improvement, it had been demonstrated that pathways could be interrupted with minimal risk and provide

1

improvement in motor control while alleviating involuntary movements. During the next 15 years, a number of targets were identified for a variety of movement disorders. Patients with intention tremor and Parkinson tremor were often considered together. Intention tremor was treated with lesions in the ventrolateral nucleus [78,79], as was hemiballismus [80]. Substantia nigra lesions were also used for hemiballismus [19,81] and hypertonus [82]. There were reports of improvement with targets in the globus pallidus [74,83]. The most common target for tremor at that time was in the ventrolateral thalamus [78,84,85]. Hyperkinesia was treated with a variety of targets [75,86,87]. Hassler [88] had not yet published his nomenclature of the subdivisions of the thalamus. The most common indication for stereotactic surgery was Parkinson’s disease. This was prior to the age of l-dopa, and pharmacologic management was not adequate. Consequently, patients were referred to the surgeon earlier in the course of the disease than now, although with more severe symptoms. The later stage bradykinesia was seen less, and patients more often presented with tremor as the primary symptom. There was no such thing as dopamine dyskinesia, and one must remember in reading the literature that the patients who were treated up to the end of the 1960s were different from the patients we see today [40]. Also some patients suffered from postencephalitic parkinsonism after the big Spanish flu epidemic in 1918, a condition which is seen only exceptionally nowadays. Irving Cooper [89] first appeared in the functional neurosurgery literature in the early 1950s. During a Walker pedunculotomy [69] for Parkinson’s disease, Cooper inadvertently interrupted the anterior choroidal artery in a now famous ‘‘surgical accident,’’ so he clipped the vessel and stopped the surgery. The patient awoke with relief of symptoms and no deficit, so, as he reported in 1953, Cooper advocated anterior choroidal ligation as a treatment for parkinsonism [89]. However, both

11

12

1

History of stereotactic surgery

the results and complications were very variable. He correctly concluded that he had often produced a stroke in an area involved with the production of parkinsonian symptoms, and the globus pallidus had been cited by others as a stereotactic target, so in 1955 he began to inject free-hand that structure with alcohol, so-called chemopallidectomy [90]. He did not use stereotactic localization (his injection guide which he introduced later was not Cartesian nor based on cerebral localization) but he reported anecdotally a relatively large series of patients. The trajectory that Cooper had selected for chemopallidectomy was through the temporal lobe, aiming upwards toward the pallidum. One patient who had a good result died of other causes, and the autopsy revealed that the needle had advanced further than intended and the lesion was actually in the ventrolateral thalamus, so Cooper moved his intended target to that area which had been introduced earlier by Hassler and Riechert. In 1958 Cooper reported a series of 700 patients contrasting chemopallidectomy and chemothalamectomy [91,92] and the series had grown to 1,000 patients by 1960 [93]. He still used alcohol injection, which was a problem, since it would spread in an uncontrolled fashion. Consequently, he changed from injection of alcohol with a brain needle to a cannula with a balloon at the tip that was intended to leave a cavity that would retain the injection material, but it did not [36]. This fared no better and its blunt tip caused damage throughout the insertion tract, so he introduced a thick injection material, Etopalin [93], but still encountered the problem of uncontrolled spread. This led him to introduce the Cryoprobe [39] in 1961 – although it had a relatively large diameter and blunt tip, it made a lesion by destroying the tissue by freezing a ball of tissue at the end of the probe, which he continued to use for the remainder of his surgical career. If we might digress, the story of the Cryoprobe provides a little-known but fascinating coincidence. The original Spiegel-Wycis report introducing human stereotactic surgery [5] in

1947 had four coauthors. In addition to Spiegel and Wycis, there was Marks, the machinist from Temple Medical School who actually made the device. The fourth author was A.St.J.Lee, who was a college student who worked as a handyman in Spiegel’s laboratory. He soon after quit his job and returned to school, completed an engineering degree and became a freelance engineering consultant. The second author on the original Cooper report of ‘‘cryostatic congelation’’ is the same Arnold St. J. Lee [39], who was coincidentally hired by Cooper to design and build the Cryoprobe. I (plg) understand that a dispute arose over who owned the patent, which was never fully resolved. By 1954, Hassler and Riechert [76] had defined their thalamic targets more precisely, with the Vop recommended for tremor and the Voa recommended for rigidity. This was made possible by Hassler’s [88] subdivision of the thalamic nuclei, so that the results of lesioning more precisely localized targets allowed better correlation with clinical results. Spiegel and Wycis [74] still preferred the pallidum as the target, and in 1958 they observed that the lesion would be more effective against rigidity if it were placed more posteriorly than the tremor target in the emerging ansa lenticularis fibers. In 1959, Svennilson and coauthors [52] reviewed Leksell’s cases and also advocated a pallidal lesion more ventral and posterior than that used by other authors (in a study later cited by Laitinen [94] that led to the rebirth of VP pallidotomy). Another interesting study was published in 1959 by Levy who was a stipendiary of the Swiss Academy of Science spending several years under the guidance of Riechert in Freiburg [95]. He compared the differences in the pallidal target used by various groups at that time. This study did not only consider the target coordinates but also the angle of the trajectory in relation to the line between the foramen of Monro and the posterior commissure. There was a large variety considering both the target in the pallidum itself

History of stereotactic surgery

but also in the attempts to include pallidofugal fibers. Hassler and colleagues considered pallidotomy to be not effective for alleviation of hypokinetic symptoms because it was thought that a negative motor symptom could not be improved by a lesion: ‘‘for theoretical reasons alone, one could hardly expect an improvement of akinesia by a stereotactic operation’’ [7,96]. Nevertheless, despite the theoretical difficulties it was occasionally acknowledged that pallidotomy indeed improved akinesia. In the late 1950s, however, most stereotacticians followed the lead of Hassler and Riechert to the thalamus, since the most dramatic effect on the early Parkinson’s disease before the l-dopa era was prompt and complete relief of tremor, the dominant symptom seen at that time. The optimal target for tremor was eventually accepted to be the Vim nucleus [75,97–99], and the pallidum was almost abandoned [100]. Meanwhile, Spiegel and Wycis [101–103] moved their lesion for Parkinson’s disease to Forel’s field, a procedure they called ‘‘campotomy,’’ for campus Foreli. In 1961, microelectrode recording (MER) from the human brain was introduced by AlbeFessard [104]. It was adopted as a surgical tool to the point where many consider it an essential technique [105–107]. A number of authors used MER to confirm localization in the Vim nucleus [54,108,109], but MER was not yet a routine part of stereotactic surgery, in part for the lack of adequate recording in the unfriendly operating room electrical environment. (It later became important in defining the subthalamic nucleus [110,111]). Both thalamotomies and pallidotomies were also popular for the treatment of dystonia in the 1960s. The results were more variable than those reported for parkinsonism [8,112] but overall beneficial results were achieved in more than 50% of patients including generalized and cervical dystonia. There is published experience with more than 300 patients with cervical dystonia [104,113]. Hassler elaborated a complex model

1

to explain the deviation of the head along its different axes including the interstitial nucleus of Cajal, the pallidum and thalamic nuclei [114,115]. According to his pathophysiological concepts, Hassler suggested choosing different targets depending on the pattern of cervical dystonia in the individual patient. In cases with rotatory torticollis, the primary target was the nucleus ventralis oralis internus and its interstitiothalamic pathway, while for treatment of horizontal torticollis pallidofugal pathways in Forel’s field H1 and the ventro-oral thalamic nuclei were approached. Working further along this concept Sano even started to use the interstitial nucleus of Cajal as a target for cervical dystonia [15,116]. The elaborate selection of surgical targets within the basal ganglia circuitry according to the phenomenology of dystonia in individual patients certainly was fascinating, although it was never conclusively shown that such superselective approaches indeed resulted in improved clinical outcome. It was estimated that by 1965 more than 25,000 functional stereotactic procedures for Parkinsonism had been performed worldwide. Things changed drastically in 1968, when l-dopa became generally available [59]. Within a few months, the number of patients with Parkinson’s disease presenting for surgery plummeted. Only a few patients with primary tremor went to stereotactic surgeons during the next few years. The number of neurosurgeons doing stereotactic surgery declined, and the field was mainly practiced by a few neurosurgeons in academic centers who enjoyed the challenge. There were three principal factors that lead to the abandonment of functional stereotactic surgery for dystonia in the late 1970s, about 10 years later than for parkinsonism. First, the general decline of movement disorders surgery at that time, second, the introduction of selective peripheral denervation by Bertrand, and third, the widespread use of botulinum toxin thereafter. It was not until the introduction of CT-directed targeting,

13

14

1

History of stereotactic surgery

then MRI targeting, and later the reintroduction of deep brain stimulation that stereotactic surgery rebounded, and it is now more active than ever [59]. Eventually, it was recognized that l-dopa is not a permanent answer to Parkinson’s disease. As the disease progresses with long-term l-dopa administration, the symptoms become more refractory and dopa dyskinesias may limit the tolerated dose [117,118]. The response to medication may vary significantly and abruptly, producing repeated on-off episodes during the day. Rigidity and akinesia may progress, and freezing episodes may intervene. By the early 1980s, a search was on for a surgical answer to these problems. In 1985, Backlund and associates [119] reported their first clinical trials of autologous transplantation of adrenal medullary tissue into the head of the caudate nucleus in two patients. They were encouraged enough to conclude that ‘‘the results merit further clinical trials.’’ Two years later, Madrazo and colleagues [120,121] reported two additional patients and cited more favorable results. Later that year they reported that they had operated on 18 patients [120]. This provoked great interest and programs were begun at a number of institutions. Unfortunately, the results were modest and of limited duration, [122–124], the surgery to retrieve one adrenal gland was stressful to this fragile group of patients, and the adrenal was sometimes found to be atrophic [125]. In addition, there were a number of complications resulting from the craniotomy, if open surgery were used [126], but few complications arose when the adrenal tissue was injected using stereotactic methods [127]. By 1991 the procedure was essentially abandoned. The idea of tissue transplantation continued to garner interest, and attention was shifted to the transplantation of fetal nigral tissue. As early as 1984, a symposium was devoted to the potential neurosurgical use of fetal cells [128]. The experimental groundwork had been done in rats in the

late 1980s [129] or MPTP-injected monkeys [130, 131]. In 1989, the first two patients to receive fetal cell transplantation for the treatment of Parkinson’s disease were reported by Lindvall [132], a multi-institutional consortium was established and others patients followed soon afterward [124]. The problems that existed with such a complex program caused interest to wane. There was considerable difficulty obtaining fetal tissue at the proper age and in the proper amounts, identification of the proper tissue in the fetal brain was difficult, coordination between the service obtaining the tissue and the implantation surgery team was expensive and elaborate, and the ultimate goal of the tissue remained in doubt [122,123,133]. The field of functional neurosurgery was otherwise quiet, through the 1970s and 1980s, except for long-established procedures primarily for pain and epilepsy [59]. There was little psychosurgery being done, mostly because of a public campaign against it [134] and the development of new psychotropic drugs, rather than any scientific reason. Let us pause in the story about stereotactic surgery for movement disorders, as we might catch up to this date the story of other fields of progress, to a great extent in technology. Stereotactic and functional neurosurgery has by its nature been dependent on advances in other fields, such as radiology and later imaging, radiotherapy, computer science, and miniaturization and implantation of electronic devices.

Persistent Pain Let us return to the birth of stereotactic surgery in 1947. Many of the earliest patients had intractable pain [135]. An aside – Spiegel always referred to such pain as ‘‘so-called intractable pain.’’ If there were a chance it might be treated, it would not be intractable, by definition, so truly ‘‘intractable’’ pain was not an indication for the treatment

History of stereotactic surgery

under discussion. I (plg) prefer not to use the term ‘‘chronic pain,’’ since it includes all longlasting pain, whether from cancer or from a noncancer (or unknown) etiology, which are two different clinical conditions managed in very different ways. Instead, I insist on the use of ‘‘persistent pain’’ if both cancer and non-cancer etiologies are discussed together [136]. Functional neurosurgical management of pain had been considered for almost a century prior to the advent of stereotactic surgery [137]. One of the prime indications was facial pain, particularly trigeminal neuralgia. In 1853, Trousseau [138] suggested that the paroxysmal activity of trigeminal neuralgia resembled epilepsy and suggested gasserian ganglionectomy, but because surgery in that area was too adventurous at that time, it was not reported formally until 1890 by Rose [139]. Horsley and coauthors [140] advocated epidural total gasserian ganglionectomy by a transsphenoidal approach in 1891, but a mortality rate of 20–25% was prohibitive, even in his excellent hands. In 1900, Cushing [141] modified the procedure, and in 1920 he reported 298 consecutive cases without mortality [142]. Ramonede [143] had already introduced the suboccipital approach in 1903, and Dandy [144] modified it in 1925. In 1931, Kirschner [145,146] introduced electrocoagulation of the gasserian ganglion. He developed an apparatus to guide the electrode through the foramen ovale, which was not Cartesian and therefore not stereotactic. His use of electrocoagulation in the human was encouraging to those who later used it in the brain. At the time that stereotactic surgery was introduced, the philosophy for pain management was to interrupt the primary pain pathway, and the most inviting target was the spinothalamic fiber bundle. Although the first patient operated with stereotactic surgery had a motor disorder, Huntington’s chorea, the second had persistent pain. Walker [26] had earlier described the surgical section of the pain pathway at the level of the mesencephalon, and Spiegel and

1

Wycis made lesions in a mesencephalotomy target [135,147], although again they made a second lesion in the dorsomedial nucleus of the thalamus, as well. Walker had reported dysesthesia from the medial lemniscus being involved with his mesencephalotomy incision, but stereotactic techniques avoided that complication. If the lateral spinothalamic tract is sectioned by open surgery in the spinal cord, the procedure is anterolateral cordotomy [148–150]. If sectioned in the brain, the spinothalamic fibers that have not already synapsed in the lower brain stem lie just behind the medial lemniscus at the level of the mesencephalon. Unfortunately, when the surgical section included the medial lemniscus, severe dysesthesia might occur [151], and that was more easily avoided with stereotactic than with open surgical techniques [152,153]. The quintothalamic fibers, which descended from the trigeminal area to join the spinothalamic bundle, provided a more compact target, so a stereotactic procedure was done for facial pain quite early [135]. Again, dorsomedial thalamotomy was often recommended to relieve the emotional component of persistent or chronic pain [154]. Thalamic pain was managed with lesions in the ventral posteromedial nucleus and the centre median nucleus [42]. In 1949, He´caen, Talairach and associates [42,155] reported on a thalamotomy for persistent pain, but they interrupted the diffuse pain projection system in the centrum medianum plus a lesion in the ventrobasal complex, demonstrating successful relief of pain without interrupting the primary pain pathway. Spiegel and Wycis [156] reported similar findings for facial pain in 1953 and further refined the procedure in 1964 by defining several distinct targets within the mediobasal thalamus [157]. The concept of interrupting the reticulospinothalamic tract for pain management led Nashold [158] in 1969 to extend the mesencephalic lesion into that bundle. This in turn led him to explore the mesencephalon with implanted electrodes to define the multisynaptic pathway [159].

15

16

1

History of stereotactic surgery

The result was to leave the primary pain pathway intact and to confine the lesion to the extralemniscal area, which provided equivalent pain relief with minimal risk of dysesthesia [151,160]. This demonstration led to the limbic system becoming a primary target for pain management. Foltz and White [161] (as reported by Sweet and Gybels [136], who previously had considerable experience with the use of cingulotomy for psychiatric disorders, began in 1962 to use that procedure for pain management. Long-term relief was reported in over half the patients with cancer pain and one-third with ‘‘failed back syndrome.’’ Although it is functional but not ordinarily stereotactic, percutaneous cervical cordotomy must be mentioned. In 1959, Mullan [162] introduced the implantation of a radioactive seed as a method for producing lesions for motor disorders, such as Parkinson’s disease. In 1963, he introduced the use of a radioactive strontium needle inserted percutaneously between the arch of the first and the lamina of the second cervical vertebrae, lain against the anterolateral surface of the spinal cord for a measured duration, in order to make a cordotomy lesion to manage pain without the need for surgical exposure [163]. This approach was used in 1965 by Rosomoff [164] who made a controlled lesion with a radiofrequency electrode, which was much more practical. This more practical procedure was adopted by many neurosurgeons. There was one grave risk, however, that of Ondine’s curse or sleep-induced apnea after bilateral lesions were made [165]. Unilateral percutaneous cervical cordotomy, however, had good results with reasonable risk, particularly in cancer patients but not particularly in patients with other persistent pain. Nevertheless, since many of the cancer patients required bilateral pain management, Lin, Polakoff and I [166] introduced in 1966 a technique to introduce the electrode through a disk to the lower cervical spinal cord, which provided good relief of bilateral pain but with occasional weakness of the hand.

Back to 1937, when Sjo¨qvist [167] presented a technique, later modified by White and Sweet [168] for surgical interruption of the descending trigeminal tract at the level of the medulla, limiting the analgesia to the distribution of the trigeminal nerve. In 1970, Hitchcock [169] made the procedure stereotactic by inserting the electrode through the foramen magnum, an approach that was uniquely suited to his stereotactic apparatus, and reported good results in postherpetic facial neuralgia. He also used that approach to modify percutaneous cervical cordotomy by inserting the electrode from dorsally through the uppermost spinal cord into the anterolateral spinothalamic tract [170], which was similar to the approach Crue and his colleagues [171] reported in 1968. This led to an inadvertent discovery of a new pain pathway [172]. One of Hitchcock’s patients reportedly moved as the electrode was inserted, and the lesion was made in the midpoint of the spinal cord at the cervico-medullary junction, with an excellent clinical result and no complications [173]. He theorized that he had interrupted a pain pathway, probably the spinoreticulothalamic multisynaptic path, and began to use the same target for pain management. He and later Schvarcz [174] termed the procedure extralemniscal myelotomy. In an attempt to avoid making a cervical lesion to treat pain confined to the pelvic area, Gildenberg and Hirshberg [175] made a mechanical lesion under surgical exposure at the thoracolumbar spinal cord level with good relief of particularly visceral cancer pain, a procedure they dubbed limited myelotomy. The spinal cord of one of the patients who had later died from his cancer was studied by Al-Cher, Willis and his group [8], who demonstrated that there was indeed a pathway, previously undescribed, not multisynaptic, transmitting pelvic visceral pain. This brings us to the point in the discussion where pain management intersects with chronic stimulation of the nervous system, the beginning of so-called neuromodulation.

History of stereotactic surgery

Neuromodulation-Stimulation There is a long history of application of electrical stimulation to the nervous system. It is reported that Scribonius treated gout pain by application of an electric torpedo fish as early as 15 AD [176]. One of the earliest to perform controlled stimulation with close observation of muscle contraction was Benjamin Franklin [177] as early as 1774, several years before Galvani [178] demonstrated electrical contraction of frog muscle in 1780. Perhaps the earliest treatise on potential physiologic use of electricity was written by Mary Shelly [179] in her novel Frankenstein, which was based on scientific speculation previously published by Dr. Erasmus Darwin, Charles Darwin’s grandfather. In 1870, Fritz and Hitzig [180] demonstrated that limb movement occurred on stimulation of the motor cortex of the dog. Electrical stimulation was applied to the brain of an awake patient soon after, in 1874, when Barthalow [181] stimulated the motor cortex that was exposed after debridement for osteomyelitis. It was left to Sir Victor Horsley [182] to first use intraoperative stimulation in 1884, when he stimulated an occipital encephalocele and noted conjugate eye movement. The first electrical stimulator designed specifically to treat pain appeared in the early 1900s when the Electreat was advertised to relieve not only pain, but innumerable physical maladies, as well. It was battery operated and bore an uncanny resemblance to TENS units that appeared 70 years later. Stimulation during stereotactic surgery was used by Spiegel and Wycis from the very first case in order to obtain physiologic localization of the electrode. Since the first lesions were in the pallidum and soon after the thalamus, stimulation was used to assure that the electrode or needle did not lie in the internal capsule by observing for a contralateral involuntary motor response. Although various frequencies were used, there

1

was not originally a distinction made between high frequency and low frequency stimulation, nor were the responses to stimulation recorded with detail. Hassler [183] was the first to suggest that observations made on stimulation in the operating room might have long-term effects. He had been a graduate student of Rudolph Hess in Switzerland during the late 1940s, where chronic stimulation was routinely administered to cats with permanently implanted electrodes. They recognized that stimulation might produce the same effects as making a lesion at the same site, but changing the frequency might give the contrasting effect. Throughout the stereotactic community, little attention was paid to high frequency versus low frequency stimulation. Those terms were not universally defined, so some institutions tested the patients with significantly different parameters. In addition, stimulation caused seizures in some rare instances, so higher frequencies were sometimes avoided. Even so, intraoperative stimulation became the norm prior to lesion production. For instance, Spiegel and Wycis [103] made lesions in Forel’s field for the treatment of Parkinson’s disease, but stimulated critically prior to lesion production. The desired target lay just above the emerging oculomotor fibers, so they stimulated at successively deeper levels until uni-ocular deviation demonstrated that they had impinged on the oculomotor fibers. The electrode was then withdrawn 2 mm and a lesion was made. Tasker [184] performed an extensive stimulation study of the human thalamus, which he published as a physiological atlas in 1982. The technique was very similar to that he used as a graduate student with Clinton Woolsey from 1961 to 1963 to map the cortex and subcortex of animals [185]. Since there was no way to apply stimulation for prolonged periods, the therapeutic potential of stimulation of the brain was rarely pursued.

17

18

1

History of stereotactic surgery

Perhaps the earliest was Pool [186] who stimulated frontal tracts rather than performing prefrontal lobotomy for psychosurgery in older patients as early as 1948. In the early 1950s, Heath [187] stimulated a variety of subcortical areas and made detailed observations about behavioral changes. In 1954, Olds and Milner [188] observed that rats would aggressively seek stimulation of the septal area, which they concluded provided the rats with intense pleasure. That same year, Heath [189] concluded that, since pleasure is the opposite of pain, septal stimulation might be used to treat pain. There were no implantable stimulators, so he stimulated the septum for intervals of 15 min daily to weekly and was able to alleviate cancer pain in one patient. A decade later, when chronic stimulation was available, Gol [190] implanted stimulators in the septal area and had relief of cancer pain in several patients. In 1972, Bechtereva [191] reported what may have been the first therapeutic use of stimulators in motor disorders. However, implantable stimulators were not available in Russia, so again the stimulation was applied to the pallidum or thalamus only intermittently. In the meantime, significant advances had been made in the understanding of pain perception. The concept that provided the basis for the use of stimulation in persistent pain was the presentation of the Melzack-Wall [192] gate theory in 1965. They proposed that pain perception involves a ‘‘gate’’ that can be opened or closed to allow pain sensation to pass through or to block it. If the activity of the small pain fibers predominates, the gate will open. If the large non-pain proprioception and touch fibers predominate, te gate will close and pain will decrease (‘‘If you rub it, it feels better!’’). Since the large non-pain fibers are isolated in the dorsal columns, stimulation of that part of the spinal cord should close the gate and provide relief of pain. Stimulating the skin with TENS unit electrodes applied to the skin and adjusting the sensation so it is below

pain threshold [193]. It could also be done by stimulating through an electrode placed behind the spinal cord (and in other positions, as it turned out), which provided the impetus to provide an implantable stimulator. The gate theory was tested in 1967 by Wall and Sweet [194] who stimulated their own infraorbital nerves. Sweet recruited Roger Avery, an engineering colleague at MIT, to make an implantable stimulator, which he and Wepsic [195] used to provide peripheral nerve stimulation for pain management. At about the same time in 1967, Norm Shealy [196] stimulated the large nerves where they were uniquely gathered in the dorsal columns of the spinal cord. He theorized that the impulse would travel retrograde down the dorsal columns to inhibit the small nerve input at each level of the spinal cord to close the gate and diminish pain sensation. He recruited Thomas Mortimer, a graduate engineering student, to design an implantable stimulator. The first mode required an external power supply connected to the stimulator by needles inserted through the skin. By coincidence, Mortimer had interviewed for a job at Medtronic 2 years before that. He contacted Norm Hagfors, one of the engineers he had met, to see if their cardiovascular stimulator might be adapted to stimulate the spinal cord. Mortimer designed an implantable electrode that Shealy used with the Medtronic cardiac stimulator, which provided relief of pain for the last several months of a cancer patient’s life. Shealy contacted Medtronic to improve and provide the system for more patients. Medtronic had previously been in the business of manufacturing implantable cardiovascular stimulators. In 1963, they were making the Barostat, which was used to stimulate the carotid sinus for treatment of hypertension. In 1965, they released the Angiostat, which stimulated the carotid sinus for angina. Shealy’s second patient used that stimulator attached to the electrode that Mortimer had designed and had good relief of chronic pain for

History of stereotactic surgery

4 years. In 1968, Medtronic provided this system for spinal cord stimulation as the Myelostat. The early spinal cord stimulators came in two parts. An internal implantable system had no internal power supply, since implantable batteries were just being developed. It was attached to a circular wound antenna implanted subcutaneously. The external unit had the controls and a battery, and transmitted both the power and the control signal transcutaneously. By 1981, battery technology had advanced to the point where the entire unit could be implanted. Avery had kept pace with Medtronic until that time, but when Roger Avery retired, the company no longer provided implantable spinal cord stimulators. In 1971, I (plg) was working at the Cleveland Clinic just down the street from where Shealy and Mortimer had introduced spinal cord stimulation. I was able to obtain stimulators from Medtronic modified to provide frequencies of 800–1,200 Hz. They were implanted to stimulate at the C2 level for the treatment of spasmodic torticollis. Half the patients had significant relief, which was the first use of implanted stimulators for motor disorders [197]. In 1976, both Cook [198] and Dooley [199] recognized improvement in spasticity in multiple sclerosis patients who had had spinal cord stimulators implanted for pain of muscle spasm. In addition, Dooley [200] recognized improvement in peripheral blood flow in patients undergoing spinal cord stimulation for pain management. It was in 1973 that Hosobuchi [201] implanted a stimulator attached to an electrode in the somatosensory thalamus for treatment of denervation pain with anesthesia dolorosa, and the field of deep brain stimulation (DBS) was born. There were few attempts during the 1970s to introduce DBS also for the treatment of movement disorders. In 1977, Mundinger reported on the benefits of unilateral thalamic DBS in seven patients with cervical dystonia [202]. Intermittent stimulation for 30–40 min with frequencies up to 150 Hz resulted in improvement of dystonia

1

for up to 7 h. The longest follow-up record was 9 months. The results were never published in the English literature and the study was completely forgotten for decades. Let us go back to 1969. Reynolds [203] demonstrated in the rat that periventricular stimulation produced profound analgesia, sufficient to perform surgery with no apparent pain perception. In 1977, Richardson and Akil [204] provided chronic periventricular stimulation to patients and produced marked reduction in pain. The following year, they demonstrated that application of such stimulation was associated with release of endorphin into the ventricular fluid [7]. Also in 1977, spinal cord stimulation and DBS were being used so extensively that the Food and Drug Administration held a symposium on safety and efficacy [205]. It was felt that the use of stimulators for pain had been documented, but not for other uses, which at that time included movement disorders, epilepsy, cerebral palsy and bladder control. At about that same time, the FDA was given the charge to regulate devices as well as their historical charge to regulate drugs. They felt that relief of pain by deep brain stimulation had not been sufficiently documented and gave the manufacturers several years to provide the data to document that such devices should be continued, especially for pain management. Of the three manufacturers, only Avery provided data, but just then Roger Avery retired so that product was discontinued, and the use of DBS for pain management was de-approved. In 1991, Tsubokawa [206] reported on the stimulation of the motor cortex, but not the sensory cortex, for the management of central pain. In 1995, Migita [207] reported on the use of extracranial magnetic stimulation of the motor cortex for pain management. As a general rule, ablative procedures are more usually indicated for cancer pain, but stimulation procedures for non-cancer persistent pain [208,209].

19

20

1

History of stereotactic surgery

In 1979, the senior author commented that the engineers could give us any stimulation parameters we wanted, but it was up to the surgeons and scientists to let them know what we need [210]. That has not changed.

The Return of Movement Disorder Surgery When l-dopa became widely used for treatment of Parkinson’s disease in 1968, stereotactic surgery was rarely used for that indication. Although there were other indications for stereotaxis, they were not enough to maintain a critical mass of centers, so stereotactic surgery went into a marked decline [59]. It was a seminal report by Laitinen [94,211] in 1992 that re-awakened interest once again in the use of pallidotomy for Parkinson’s disease, and with that awakened the field of stereotactic and functional neurosurgery. It had become obvious that many of the patients who took l-dopa for years were still disabled and needed a more aggressive therapy. Even more, it was recognized that chronic l-dopa treatment resulted in disabling dyskinesias and unpredictable motor fluctuations. Laitinen recalled the report of Leksell’s pallidotomy that had been published in 1960 by Svennilson and associates [52] who had reported more improvement in bradykinesia and rigidity with a lesion that Leksell had made in the ventral posterior area of the pallidum than with the more central lesion. He attributed this observation to the inclusion of the pallidofugal fibers in the lesion, similar to Spiegel and Wycis [212] pallido-ansotomy. After a cautious start in 1987, Laitinen and his colleagues [94,211] reported in 1992 a significant improvement in rigidity, bradykinesia and dopa-induced dyskinesia in patients who had been taking l-dopa for years for their Parkinson’s disease. There was an enthusiastic return to stereotactic pallidotomy for Parkinson’s disease [213]. The setting was more advanced than had

existed in the original years of surgical management of Parkinson’s disease. The evaluation of results was more sophisticated [214], localization of the target had presumably become more accurate with the introduction of imaging techniques [215], and microelectrode confirmation of the target [216] may have helped to localize the lesion. In addition, it was found that pallidotomy managed not only the symptoms of Parkinson’s disease, but the side-effects of l-dopa, such as dyskinesia. The first ‘‘modern’’ pallidotomy in the United States was performed in December, 1991, in the Hospital for Joint Diseases, New York, by Michael Dogali [217] in the presence of Laitinen and Tasker. Dogali initially considered the possibility of placing lesions in the subthalamic nucleus after reading reports on the experimental studies of the Atlanta group and discussed this issue with Ransohoff. As a neurosurgeon who had actively participated in the first wave of functional stereotactic surgery, however, Ransohoff strongly opposed using the subthalamic nucleus because of the fear of producing hemiballism and instead suggested using the pallidum. Many pallidotomy series were reported over the next 5 years [213,218]. Many of the neurologists who referred such patients became involved in the intraoperative microelectrode evaluation of targets [216], further encouraging referral of patients. The resurgence in stereotactic activity also led to a search for new targets. Improvements in imaging during the prior decade made target visualization more feasible. Improvements in physiological localization allowed the surgeons to be more secure in identifying targets. Prior to the lull, lesions had been placed by a few adventurous neurosurgeons in the zona incerta [219] and the subthalamic nucleus [220], which became a target for DBS. In 1980, during the lull, Brice and McLellan [221] used thalamic stimulators in two patients for management of tremor of multiple sclerosis. Also during the lull, the following year, Benabid and his colleagues [222] reported on management of tremor by deep brain stimulation

History of stereotactic surgery

(DBS) in the Vim nucleus. In 1994, when Siegfried and Lippitz [223] reported on chronic electrical stimulation of the VL-VPL complex and of the pallidum, they indicated that this represented their experience since 1982. Benabid carried the banner for the use of DBS in motor disorders and popularized the field by his results and the study of the effects of DBS on various targets. Based on laboratory studies that stimulation of the subthalamic nucleus improves the symptoms of Parkinson’s disease, they have concentrated on this target, which has become the primary target for such stimulation [224]. Since the effects of moderately high frequency stimulation are equivalent, the targets for stimulation are for the most part the same than the targets where lesions are made. In those areas where DBS is not generally available, the success of subthalamic stimulation has led to renewed interest in lesioning targets [225]. Other targets have presented themselves, in part because the risk of permanent complications are less with stimulation than with lesions, so surgeons can be more adventurous. Velasco and his group [226] stimulate the prelemniscal radiations with success, a target just lateral to the old campotomy target [227]. DBS has become increasingly popular in Europe during the past decade and in the US since it was approved in 2002 [72,228]. The renaissance of functional stereotactic surgery for dystonia occurred with a delay of about a decade after that of Parkinson’s disease. With that consideration, we have to remember that also the decline of dystonia surgery happened a decade later than that for Parkinson’s disease in the 1970s. Encouraged by the improvement of dyskinesias in Parkinson’s disease patients after pallidotomy, the GPi was reintroduced as a target for radiofrequency lesioning in the early and mid 1990s [112], While it was shown that pallidotomy yielded beneficial results, it became also clear very soon, however, that bilateral surgery which is necessary in dystonia

1

was burdened with a higher frequency of side effects and that the improvement of dystonia lessened after years. Therefore, pallidal DBS was introduced in the mid 1990s for cervical dystonia [229] and generalized dystonia [230,231].

Epilepsy Surgery Let us go back in time again. Epilepsy also invited a variety of approaches [232–234]. Lesions were often made in the targets that had been defined from movement disorders, on the theory that both represented uncontrolled activation that might be propagated through known pathways. Forel’s field was one of those areas, with significant decrease in seizures being reported as early as 1963 [235]. Thalamotomy was used for myoclonic epilepsy [236]. Fornicotomy was used for epilepsy by several investigators [232,237]. Starting in the 1960s, electrodes were inserted for prolonged recording over several days to identify epileptic foci [238]. The hallmark of surgery for epilepsy remained temporal lobectomy in selected patients [239,240], or the more selective amygdalotomy [241], which was made even more precise with image guidance [242], which is discussed below. With image guidance, it was possible to insert a multi-contact depth electrode from occipitally just lateral to the hippocampus through the temporal lobe to its tip, as well as subdural electrode strips over the anterolateral surface and just beneath the temporal lobe. Prolonged recording identified which contact lay at the origin of the seizures. That contact could then be approached also with image guidance to obtain the optimal temporal lobe resection [243].

Psychiatric Surgery Again we go back in time. In the late 1930s and 1940s, pre-frontal lobotomy was introduced as being beneficial for psychiatric disorders [20].

21

22

1

History of stereotactic surgery

The indications, however, were not clear and it is very likely that many of those patients had schizophrenia, which does not respond to psychosurgery. There were no psychotropic medications other than barbiturates, and often the only alternative to surgery was for permanent commitment to a mental institution. Pre-frontal lobotomy produced poorly controlled damage to the frontal lobes, and it became over-used and abused [244]. During the 1950s, pre-frontal lobotomy became less desirable than it had been, in part because new medications became available and stereotaxis provided a better controlled alternative. The first stereotactic patient had dorsomedian thalamotomy [5]. Dorsomedian lesions were combined with lesions in the anterior nuclei for anxiety and aggressive disorders [245]. Lesions of the internal medullary lamina were again combined with hypothalamic lesions for aggressive behavior [246–248]. Surgery for psychiatric symptoms almost came to a halt in the late 1970s and through the 1980s for what appeared to a great extent for political rather than scientific reasons. As occurred during that period, protests were used to interrupt scientific meetings where psychiatric surgery was being discussed, and all surgery for psychiatric symptoms was equated in the media with the non-anatomical and abused psychosurgery of the pre-stereotactic era [134,249]. Although psychiatric surgery has resumed on a more limited basis, the availability of psychotropics and more specific psychiatric diagnosis has put it on a more scientific basis. The main indications are now recognized as obsessive-compulsive disorder [250,251] and intractable depression [252,253]. As with motor disorders, there appears to be a significant role for deep brain stimulation [254,255].

Image Guided Surgery After the first generation of stereotactic frames, there was little further modification until the late

1970s, with the introduction of image guided surgery [59]. The idea of using X-ray visualization to identify the location of radio-opaque masses is older than you think. Perhaps the birth of image guided surgery can be traced to the work of Elizabeth Fleishmann in San Francisco in 1900 [256]. When she was 28 years old, Roentgen’s discovery of X-rays captured the public’s attention, and do-it-yourself articles appeared in the newspapers. She quit her job as a bookkeeper and somehow managed to set up a complete X-ray system in an office in Sutter Street the following year. She became perhaps the best radiologist on the west coast. Soldiers returning from the Spanish-American War in 1900 were referred to her to identify bullets and shrapnel that they still carried. She developed the skill to triangulate on bullets lodged in the skull or body and to steer surgeons to them so they might be removed. She certainly qualifies as being the mother of image guided surgery. Up until CT scanning was introduced, intracerebral masses were deduced from shifts in blood vessels in angiography or the position of the ventricles in ventriculography. Now for the first time it was possible to see the mass itself, which invited stereotactic intervention as early as 1956 [257]. New techniques had to be developed to relate the target to stereotactic coordinates in order to guide the stereotactic frame with CT images rather than X-ray [258,259]. Each slice of the CT scan presented a measurable two-dimensional picture from which AP and lateral coordinates could be measured. The relative position in space of the target slice provided the third vertical coordinate. By localizing that slice on the head in order to register it to the stereotactic apparatus, the third coordinate could be determined. A biopsy cannula or other probe could be inserted in order to direct the surgeon to the pathology [260]. New stereotactic devices were developed to automate that process. The Leksell apparatus was

History of stereotactic surgery

modified with a base plate that could be secured to the scanner and then to the head frame in the operating room to transpose the coordinates to the stereotactic apparatus [261]. Another system employed a series of wires of varying lengths incorporated into plastic plates attached to the head frame. The number of wires appearing in cross-section in the target slice indicated its vertical position [262]. One ingenious system used three acrylic screws with lead markers that were secured to the patient’s skull prior to scanning in order to establish a reference plane. The base ring of the stereotactic apparatus was attached to the screws, and coordinates were calculated [263,264]. Several stereotactic devices were developed especially for use with CT (and later MRI) scanning. Some depended on the calibrated movement of the CT scanner table to establish the vertical coordinate [262,265]. A CT scanner that incorporated a stereotactic apparatus was designed [266]. In some busy neurosurgical services, a CT scanner was installed in the operating room [267]. The breakthrough in marrying to stereotactic frames CT or MRI scans, as well as more recent scanners, involved the development in 1980 of a fiducial system that contains all the three-dimensional information for targeting independently on each CT slice. The idea was invented by a medical student, who is the ‘‘B’’ in the BRW apparatus [268]. Three sets of three rods, with each set in an N-shaped configuration, are attached to a frame that is in turn attached to the stereotactic head ring. Since the center rod of each set is diagonal, the height of the slice scan be determined by the position of the center rod relative to the vertical rods on each side of it. Since there are three sets of rods, three points are used to determine the position of the plane bearing the target, and the AP and lateral coordinates can be established on that target slice. This system was first incorporated into the BRW system, a frame consisting of interlocking arcs, and

1

similar systems have been used with other apparatus as well [115,269,270]. The availability of image-based stereotactic surgery opened up new possibilities for management of brain tumors and other masses, and brought many neurosurgeons into the stereotactic arena. The most common stereotactic procedure became biopsy [63]. In addition, aspiration of abscesses [271], hematomas [272,273], and cysts [274] became commonplace. A stereotactic frame could be used to guide the patient to a tumor at craniotomy [275], with a virtual reality program visualizing the tumor beneath the surface prior to making the skin incision. Visualization of structures such as the ventricle and blood vessels can guide the surgeon. The image is upgraded as the resection proceeds, so the surgeon can see when the optimal resection has been done. Cannulas [276] or isotope seeds [277] can provide brachytherapy of various types. Kelly [269,278] is considered by many to be the father of image guided brain tumor resection. His development between 1980 and 1983 of a stereotactic frame that integrated visual guidance technology antedated frameless systems and opened the door to guided resection. The data from a CT scan or MRI was fed into a computer workstation. The computer reconstructed the volume of the target, ordinarily a tumor, into a three-dimensional volumetric object that could be registered to the stereotactic head frame, rather than a target point-in-space, as had been the practice until then. The digital manipulations of those data were even more remarkable when one considers the capability of computers of that time, which required an entire room to manage the data for a single surgery. The registration of the microscope to the patient was done by aligning the view with a cylindrical retractor. The outline of the tumor was seen on a heads-up display superimposed on the microscope view. The image was manipulated so only the crosssection of the part of the tumor being resected was seen on the display. Because of the restricted

23

24

1

History of stereotactic surgery

access through the cylinder retractor, the resection was usually done with the CO2 laser [279–281]. Several technologies for frameless image guided surgery emerged at about the same time. Since most were developed or at least used commercially early in development, much of the relevant information does not appear in any detail in the scientific literature. The first frameless systems, which became generally available about 1990, consisted of an articulated arm attached to the operating table. Each of the joints contained a potentiometer to measure the angle of each single joint. The information from all the joints could then be used to calculate the position of the tip of the pointer at the end of the arm. It was used first to register the position of the patient’s head to the arm, after which the location of the tip of the pointer in relation to the head and the target could be displayed to the surgeon in real time [282]. The original use of the operating microscope as a frameless guidance instrument was developed by Roberts [283] as early as 1986. It localized its position in space by ultrasound triangulation. However, ultrasound localization had the drawback of being subject to error from air currents or temperature gradients in the operating room. Kelly [284] introduced frameless electromagnetic localization to image guided surgery, first with the Regulus Navigator, then with his Compass system which eventually required only a lap top computer for neuronavigation. The most commonly used localization system at present involves the localization in space of a series of computer identifiable fiducials by a pair of video-like cameras overlooking the surgical field, reported by Heilbrun [285] in 1992 as machine vision. By 1994, his team reported the use of this system for multiple imaging modalities [286,287]. This system was used by Smith and Bucholz [288] in 1994 in a system they called the NeuroStation that grew up to be the Stealth Station,

now the most widely used neuronavigation system in the US (the most widely used system in Europe is the BrainLab system). Fiducials are secured to the patient’s head prior to scanning. A three-dimensional reconstruction of the head, including the fiducials, is computed. In the operating room, the surgeon localizes each of the fiducials sequentially by touching each in turn with the image localized pointer, which registers the location of the patients head to the preoperative volumetric scan. Thereafter, the surgeon can use the tip of the pointer to localize any structure of interest or to localize the tip of the pointer in relation to the target even before the incision is made. More recently, the development of computer-generated skin surface rendering has become an alternative to the use of fiducials. Other authors have used similar threedimensional volume reconstruction as early as 1994 to guide craniotomy and tumor resection by a system that visualizes the entire volume of the target, volume-in-space rather than a pointin-space [275,289–291]. The system that has been used by Gildenberg [275,292,293] localizes a video camera stereotactically, so that the video image of the surgical field is registered to the reconstructed volume of the tumor. The superimposition of both images provides virtual reality to surgical resection.

Further Steps The history of stereotactic and functional neurosurgery has been documented in the ‘‘stereotactic journal’’ as it occurred. When Spiegel first reported the birth of human stereotactic surgery in 1947, he was editor of the journal Confinia neurologica, where a preponderance of early articles was published. When Spiegel retired in 1968, Gildenberg became editor and changed the name to Applied Neurophysiology, since that described almost all of the functional procedures that constituted the field. Within a few years,

History of stereotactic surgery

image guidance, computers, and stereotactic radiosurgery became part of the field, and the name was changed to Stereotactic and Functional Neurosurgery. Half of the issues between 1968 and 2001 were devoted to proceedings of the World and American Societies for Stereotactic and Functional Neurosurgery. The philosophy was based on the feeling that if anyone wanted to keep up with the field, he or she would know what was happening in the field by reading just this one journal, a repository of stereotactic history as it happened [294]. The journal is stronger than ever under the editorial leadership of David Roberts since 2001. Stereotactic and functional neurosurgery nowadays is a major column supporting the building of neurosurgery. Its concepts have penetrated essentially all subspecialties of neurosurgery and they reach far beyond to other disciplines. Therefore, the question arises how the core of contemporary stereotactic and functional neurosurgery would be defined. In an attempt to establish a Training Chart in Movement Disorders Surgery Added Competence by the ESSFN the first request by the public authorities was to give a precise and pragmatic definition of the field nowadays. After a long discussion the following definition came up as a consensus based on the input of Drs. Blond, Broggi, Gildenberg, Hariz, Krauss, Lazorthes and Lozano: "

Stereotactic and functional stereotactic surgery is a branch of neurosurgery that utilizes dedicated structural and functional neuroimaging to identify and target discrete areas of the nervous system and to perform specific interventions (for example neuroablation, neurostimulation, neuromodulation, neurotransplantation, and others) using dedicated instruments and machinery in order to relieve a variety of symptoms of neurological and other disorders and to improve function of both the structurally normal and abnormal nervous system. The practice of stereotactic and functional neurosurgery mainly extends

1

into the fields of movement disorders, pain, epilepsy, psychoaffective disorders, neoplastic diseases of the nervous system and the restoration of function in degenerative disorders.

References 1. Gildenberg PL. General concepts of stereotactic surgery. In: Lunsford LD, editor. Modern stereotactic neurosurgery. Boston: Martinus Nijhoff; 1988. p. 3-12. 2. Horsley V, Clarke RH. The structure and functions of the cerebellum examined by a new method. Brain 1908;31:45-124. 3. Descartes R. Discours de la me´thod pour bien conduire sa raison et chercher la ve´rite´ dans les sciences. Leyden, Holland: Maire; 1637. 4. Pereria EAC, Green AL, Nandi D, Aziz TZ. Stereotactic surgery in the United Kingdom: the hundred years from Horsley to Hariz. Neurosurgery 2008 (in press). 5. Spiegel EA, Wycis HT, Marks M, Lee AS. Stereotaxic apparatus for operations on the human brain. Science 1947;106:349-50. 6. Frankfort plane. Dorlandaˆ s Illustrated Medical Dictionary. Philadelphia, PA: W.B.Saunders; 1994, p 1300. 7. Akil H, Richardson DE, Hughes J, Barchas JD. Enkephalin-like material elevated in ventricular cerebrospinal fluid of pain patients after analgetic focal stimulation. Science 1978;201:463-5. 8. Al Chaer ED, Lawand NB, Westlund KN, Willis WD. Pelvic visceral input into the nucleus gracilis is largely mediated by the postsynaptic dorsal column pathway. J Neurophysiol 1996;76:2675-90. 9. Clarke RH. Part I. Investigation of the central nervous system, methods and instruments. Baltimore: Johns Hopkins; 1920. 10. Levy R. A short history of stereotactic neurosurgery. Park Ridge, IL: American Association of Neurological Surgeons; 1992. 11. Schaltenbrand G. Personal observations on the development of stereotaxy. Confin Neurol 1975;37:410-6. 12. Olivier A, Bertrand G, Picard C. Discovery of the first human stereotactic instrument. Appl Neurophysiol 1983;46:84-91. 13. Dittmar C. Ueber die Lage des sogenannten Gefaesszentrums in der Medulla oblongata. Ber saechs Ges Wiss Leipzig (Math Phys) 1873;25:449-69. 14. Zernov DN. Encephalometer. Device for estimation of parts of brain in human (Russian). Proc Soc Physicomed, Moscow Univ 1889;2:70-80. 15. Altukhov NV. Encephalometric investigations of the brain relative to the sex, age and skull indexes. Moscow; 1891.

25

26

1

History of stereotactic surgery

16. Gildenberg PL. ‘‘Stereotaxic’’ versus ‘‘stereotactic’’. Neurosurgery 1993;32:965-6. 17. Gildenberg PL. Ernest A. Spiegel 1895–1985. Appl Neurophysiol 1985;48:I-VI. 18. Gildenberg PL. Spiegel and Wycis – the early years. Stereotact Funct Neurosurg 2001;77:11-16. 19. Spiegel EA, Wycis HT. Sterencephalotomy, Part II. Philadelphia, PA: Grune & Stratton; 1962. 20. Freeman W, Watts JW. Psychosurgery: intelligence, emotional and social behavior following prefrontal lobotomy for mental disorders. Springfield, IL: Charles C Thomas; 1942. 21. Spiegel EA, Wycis HT. Stereoencephalotomy, Part I. New York: Grune & Stratton; 1952. 22. Meyers R. The modification of alternating tremors, rigidity and festination by surgery of the basal ganglia. Res Publ Ass Res Nerv Ment Dis 1942;21:602-65. 23. Meyers R. Historical background and personal experiences in the surgical relief of hyperkinesia and hypertonus. In: Fields W editor. Pathogenesis and treatment of parkinsonism. Springfield, IL: Charles C Thomas; 1958. p. 229-70. 24. Dogliotti M. First surgical sections, in man, of the lemniscal lateralis (pain-temperature path) at the brain stem, for the treatment of diffuse rebellious pain. Anesth Analg 1938;17:143-5. 25. Schwartz HG, O’Leary JL. Section of the spinothalamic tract in the medulla with observations on the pathways for pain. Surgery 1941;9:183-93. 26. Walker AE. Relief of pain by mesencephalic tractotomy. Arch Neurol Psychiat 1942;48:865-83. 27. Keele KD. Anatomies of pain. Baltimore, MD: Williams & Wilkins; 1949. 28. Livingston WK. Pain mechanisms. New York: Macmillan; 1943. 29. Talairach J, David M, Tournoux P, Corredor H, Kvasina T. Atlas d’anatomie stereotaxique. Paris: Masson; 1957. 30. Spiegel EA, Wycis HT. Pallido-thalamotomy in chorea. Arch Neurol Psychiatry (Chicago) 1950;64:495-6. 31. Gildenberg PL. The birth of stereotactic surgery: a personal retrospective. Neurosurgery 2004;54:199-208. 32. Spiegel EA. Guided brain operations. Basel: Karger; 1982. 33. Narabayashi H, Okuma T. Procaine oil blocking of the globus pallidus for the treatment of rigidity and tremor of parkinsonism. Proc Jpn Acad 1953;29:310-8. 34. Narabayashi H, Shimazu H, Fujita Y, Shikiba S, Nagao T, Nagahata M. Procaine-oil-wax pallidotomy for double athetosis and spastic states in infantile cerebral palsy. Neurology 1960;10:61-9. 35. Cooper IS. Chemopallidectomy and chemothalamectomy for parkinsonism and dystonia. Proc R Soc Med 1959;52:47-60. 36. Gildenberg PL. Studies in stereoencephalotomy. X. Variability of subcortical lesions produced by a heating electrode and Cooper’s balloon-cannula. Confin Neurol 1960;20:53-65.

37. Obrador S, Dierssen G. Cirurgia de la region palidal. Revta Clin Esp Ano XVII 1956;61:229-37. 38. Cosman ER, Nashold BS, Jr, Bedenbaugh P. Stereotactic radiofrequency lesion making. Appl Neurophysiol 1983;46:160-6. 39. Cooper IS, St Lee AJ. Cryostatic congelation. J Nerv Ment Dis 1961;133:259-63. 40. Gildenberg PL. Functional neurosurgery. In: Schmidek HH, Sweet WH, editors. Operative neurosurgical techniques, vol. II. New York: Grune & Stratton; 1982. p. 993-1043. 41. Leksell L. A stereotaxic apparatus for intracerebral surgery. Acta chir scand 1949;99:229-33. 42. He´caen H, Talairach J, David M, Dell MD. Coagulations limite´es du thalamus dans les algies du syndrome thalamique. Rev Neurol (Paris) 1949;81:917-31. ¨ ber ein neues Zielgeraet zur 43. Riechert T, Wolff M. U intrakraniellen elektrischen Abteilung und Ausschaltung. Arch Psychiatr Z Neurol 1951;186:225-30. 44. Bailey P, Stein SN. A stereotaxic apparatus for use on the human brain. Atlantic City: AMA Scientific Exhibit; 1951. 45. Narabayashi H. Stereotaxic instrument for operation on the human basal ganglia. Psychiatr Neurol Jpn 1952;54:669-71. 46. Uchimura Y, Narabayashi H. Stereoencephalotom. Psychiatr Neurol Jpn 1951;52:265. 47. Ohye C, Fodstad H. Forty years with Professor Narabayashi. Neurosurgery 2004;55:222-6. 48. Talairach J, He´caen M, David M, Monnier M, Ajuriaguerra J. Recherches sur la coagulation therapeutique des structures sous-corticales chez l’homme. Rev Neurol 1949;81:4-24. 49. Guiot G, Brion S, Fardeau M, Bettaier A, Molina P. Dyskinesie volitionelle d’attitude suppremee par la coagulation thalamo-capsulaire. Rev Neurol 1960; 102:220-9. 50. Riechert T, Wolff M. Die Entwicklung u. klinische Bedeutung der gezielten Hirnoperationen. Med Klin 1951; 46:609-11. 51. Gillingham FJ. Small localized lesions of the internal capsule in the treatment of the dyskinesias. Conf Neurol 1962;22:385-92. 52. Svennilson E, Torvik A, Lowe R, Leksell L. Treatment of parkinsonism by stereotactic thermolesions in the pallidal region. A clinical evaluation of 81 cases. Acta Psychiatr Neurol Scand 1960;35:358-77. 53. Rossi GF, Colicchio G, Gentilomo A, Scerrati M. Discussion on the causes of failure of surgical treatment of partial epilepsies. Appl Neurophysiol 1978;41:29-37. 54. Bertrand G, Jasper H. Microelectrode recording of unit activity in the human thalamus. Confin Neurol 1965;26:205-8. 55. Velasco Suarez MM, Escobedo FR. Stereotaxic intracerebral instillation of dopa. Confin Neurol 1970; 32:149-57.

History of stereotactic surgery

56. Bechtereva NP, Bondartchuk AN, Smirnov VM, Meliutcheva LA, Shandurina AN. Method of electrostimulation of the deep brain structures in treatment of some chronic diseases. Confin Neurol 1975;37:136-40. 57. Kandel EI. Experience with the cryosurgical method in production of lesions of the extrapyramidal system. Confin Neurol 1965;26:306-9. 58. Bullard DE, Nashold BSJ. Evolution of principles of stereotactic neurosurgery. Neurosurg Clin N Am 1995;6:27-41. 59. Gildenberg PL. Whatever happened to stereotactic surgery? Neurosurgery 1987;20:983-7. 60. Spiegel EA. Methodological problems in stereoencephalotomy. Confin Neurol 1965;26:125-32. 61. Spiegel EA. History of human stereotaxy (stereoencephalotomy). In: Schaltenbrand G, Walker AE, editors. Stereotaxy of the human brain. Anatomical, physiological and clinical applications. Stuttgart/New York: Georg Thieme Verlag; 1982. p. 3-10. 62. Gildenberg PL. Survey of stereotactic and functional neurosurgery in the United States and Canada. Appl Neurophysiol 1975;38:31-7. 63. Gildenberg PL, Franklin P. Survey of CT-guided stereotactic surgery. Appl Neurophysiol 1985;48:477-80. 64. Bucy PC, Buchanan DN. Athetosis. Brain 1932;55:479-92. 65. Bucy PC. Cortical extirpation in the treatment of involuntary movements. In: Putnam TJ, editor. The diseases of the basal ganglia. New York: Hafner Publishing Co; 1966. p. 551-95. 66. Bucy PC, Case TJ. Tremor. Physiologic mechanism and abolition by surgical means. Arch Neurol Psychiat 1939;41:721-46. 67. Putnam TJ. Treatment of athetosis and dystonia by section of the extrapyramidal motor tracts. Arch Neurol Psychiatry 1933;29:504-21. 68. Walker AE. Cerebral pedunculotomy for the relief of involuntary movements. I. Hemiballismus. Acta Psychiatr Neurol Scand 1949;24:712-29. 69. Walker AE. Cerebral pedunculotomy for the relief of involuntary movements. Parkinsonian tremor. J Nerv Ment Dis 1952;116:766-75. 70. Guiot G, Pecker J. Tractotomie mesencephalique anterieure pour tremblement parkinsonien. Rev Neurol Suppl 1949;1:387. 71. Dandy WE. Changes in our conceptions of localization of certain functions in the brain. Am J Physiol 1930;93:643-7. 72. Gildenberg PL. Evolution of basal ganglia surgery for movement disorders. Stereotact Funct Neurosurg 2006;84:131-5. 73. Meyers R. Dandy’s striatal theory of the ‘‘center of consciousness’’; surgical evidence and logical analysis indicating its improbability. Arch Neurol Psychiat 1951;65:659-71. 74. Spiegel EA, Wycis HT, Baird HW, III. Long range effects of electropallido-ansotomy in extrapyramidal and convulsive disorders. Neurology 1958;8:734-40.

1

75. Mundinger F, Riechert T. Die stereotaktischen Hirnoperationen zur Behandlung extrapyramidaler Bewegungssto¨rungen (Parkinsonismus und Hyperkinesen) und ihre Resultate. Postoperative und Langzeitergebnisse der stereotaktischen Hirnoperationen bei extrapyramidalmotorischen Bewedunasstro¨rungen. Teil B. Fortschr Neurol Psychiatr 1963;31:69-120. 76. Hassler R, Riechert T. Indikationen und Lokalisationsmethode der gezielten Hirnoperationen. Nervenarzt 1954;25:441-7. 77. Spiegel EA, Wycis HT. Ansotomy in paralysis agitans; demonstration of results by motion pictures and electromyograms. Trans Am Neurol Assoc 1953;3:178-80. 78. Krayenbuhl H, Yasargil MG. Relief of intention tremor due to multiple sclerosis by stereotaxic thalamotomy. Conf Neurol 1962;22:368-74. 79. Obrador S, Dierssen G. Observations on the treatment of intentional and postural tremor by subcortical stereotaxic lesions. Confin Neurol 1965;26:250-3. 80. Tsubokawa T, Moriyasu N. Lateral pallidotomy for relief of ballistic movement – its basic evidences and clinical application. Confin Neurol 1975;37:10-15. 81. Andy OJ. Diencephalic coagulation in the treatment of hemiballism. Conf Neurol 1962;22:346-50. 82. Meyers R, Fry WJ, Fry FJ, Dreyer LL, Schultz DF, Noyes RF. Early experiences with ultrasonic irradiation of the pallidofugal and nigral complexes in hyperkinetic and hypertonic disorders. J Neurosurg 1959;16:32-54. 83. Obrador S. A simplified neurosurgical technique for approaching and damaging the region of the globus pallidus in Parkinson’s disease. J Neurol Neurosurg Psychiatr 1957;20:47-9. 84. Van Buren JM, Li CL, Shapiro DY, Henderson WG, Sadowsky DA. A qualitative and quantitative evaluation of parkinsonians three to six years following thalamotomy. Confin Neurol 1973;35:202-35. 85. Yoshida M, Okada K, Watanabe M, Kuramoto S. Analysis of tremulous movements after thalamotomy correlated to intrathalamic therapeutic lesions. Appl Neurophysiol 1976;39:311-4. 86. Krayenbuhl H, Siegfried J. Dentatotomies or thalamotomies in the treatment of hyperkinesia. Confin Neurol 1972;34:29-33. 87. Riechert T. The stereotactic technique and its application in extrapyramidal hyperkinesia. Confin Neurol 1972;34:325-30. 88. Hassler R. Architectonic organization of the thalamic nuclei. In: Schaltenbrand G, Walker AE, editors. Stereotaxy of the human brain. Stuttgart/New York: Georg Thieme Verlag; 1982. p. 140 -80. 89. Cooper IS. Ligation of the anterior choroidal artery for involuntary movements of parkinsonism. Psychiat Quart 1953;27:317-9. 90. Cooper IS. Chemopallidectomy. Science 1955;121:217. 91. Cooper IS. Clinical results and follow-up studies in a personal series of 300 operations for parkinsonism. J Am Geriat Soc 1956;4:1171-81.

27

28

1

History of stereotactic surgery

92. Cooper IS, Bravo GJ. Implications of a five year study of 700 basal ganglia operations. Neurology 1958;8:701-17. 93. Cooper IS. Results of 1000 consecutive basal ganglia operations for parkinsonism. Ann Intern Med 1960;52:483-99. 94. Laitinen LV, Bergenheim AT, Hariz MI. Leksell’s posteroventral pallidotomy in the treatment of Parkinson’s disease. J Neurosurg 1992;76:53-61. 95. Levy A. Die Pallidotomie beim Parkinson syndrom. Eine vergleichende anatomoradiologische Studie. Arch Psychiatr Nervenkr 1959;199:487-507. 96. Hassler R, Mundinger F, Riechert T. The future of therapy in parkinsonism. In: Hassler R, Mundinger F, Riechert T, editors. Stereotaxis in Parkinson syndrome. New York: Springer; 1979. p. 236-48. 97. Kelly PJ, Ahlskog JE, Goerss SJ, Daube JR, Duffy JR, Kall BA. Computer-assisted stereotactic ventralis lateralis thalamotomy with microelectrode recording control in patients with Parkinson’s disease. Mayo Clin Proc 1987;62:655-64. 98. Riechert T. Long term follow-up of results of stereotaxic treatment of extrapyramidal disorders. Conf Neurol 1962;22:356-63. 99. Tasker RR, Siqueira J, Hawrylshyn P, Organ LW. What happened to Vim thalamotomy for Parkinson’s disease? Appl Neurophysiol 1983;46:68-83. 100. Levy A. Stereotaxic brain operations in Parkinson’s syndrome and related motor disturbances. Comparison of lesions in the pallidum and thalamus with those in the internal capsule. Confin Neurol 1967;291-70. 101. Spiegel EA. Significance of Forel’s field for neurosurgery and neurophysiology. Acta Neurochir (Wien) 1965;13: 292-304. 102. Spiegel EA, Wycis HT, Szekely EG, Baird HW, III, Adams J, Flanagan M. Campotomy. Trans Am Neurol Assoc 1962;87:240-2. 103. Spiegel EA, Wycis HT, Szekely EG, Soloff L, Adams J, Gildenberg P, Zanes C. Stimulation of Forel’s field during stereotaxic operations in the human brain. Electroencephalogr Clin Neurophysiol 1964;16:537-48. 104. Albe-Fessard D, Arfel G, Guiot G, Hardy J, Hertzog E, Aleonard P. Identification et de´limitation pre´cise de certaines structures souscorticales de l’homme par l’electrophysiologie. CR Acad Sci (Paris) 1961;243:2412-4. 105. Narabayashi H, Gildenberg PL, Franklin PO (eds.). Proceedings of the meeting on the use of microphysiological recordings during stereotactic neurosurgery. Stereotac Funct Neurosurg 1989;52:77-261. 106. Narabayashi H, Ohye C. Importance of microstereoencephalotomy for tremor alleviation. Appl Neurophysiol 1980;43:222-7. 107. Ohye C, Narabayashi H. Physiological study of presumed ventralis intermedius neurons in the human thalamus. J Neurosurg 1979;50:290-7. 108. Kelly PJ. Microelectrode recording for the somatotopic placement of stereotactic thalamic lesions in the

109.

110.

111.

112.

113.

114.

115.

116.

117.

118.

119.

120.

121.

122.

treatment of parkinsonian and cerebellar intention tremor. Appl Neurophysiol 1980;43:262-6. Tasker RR, Lenz F, Yamashiro K, Gorecki J, Hirayama T, Dostrovsky JO. Microelectrode techniques in localization of stereotactic targets. Neurol Res 1987;9:105-12. Falkenberg JH, McNames J, Favre J, Burchiel KJ. Automatic analysis and visualization of microelectrode recording trajectories to the subthalamic nucleus: preliminary results. Stereotact Funct Neurosurg 2006;84:35-44. Starr PA, Christine CW, Theodosopoulos PV, Lindsey N, Byrd D, Mosley A, Marks WJ, Jr. Implantation of deep brain stimulators into the subthalamic nucleus: technical approach and magnetic resonance imagingverified lead locations. J Neurosurg 2002;97:370-87. Ondo WG, Krauss JK. Surgical therapies for dystonia. In: Brin MF, Comella CL, Jankovic J, editors. Dystonia: etiology, clinical features and treatment. Philadelphia, PA: Lippincott Williams & Wilkins; 2004. p. 125-47. Loher TJ, Pohle T, Krauss JK. Functional stereotactic surgery for treatment of cervical dystonia: review of the experience from the lesional era. Stereotact Funct Neurosurg 2004;82:1-13. Hassler R, Dieckmann G. Stereotactic treatment of different kinds of spasmodic torticollis. Confin Neurol 1970;32:135-43. Alker G, Kelly PJ. An overview of CT based stereotactic systems for the localization of intracranial lesions. Comput Radiol 1984;8:193-6. Sano K, Sekino H, Tsukamoto Y, Yoshimasu N, Ishijima B. Stimulation and destruction of the region of the interstitial nucleus in cases of torticollis and see-saw nystagmus. Confin Neurol 1972;34:331-8. Crossman AR. A hypothesis on the pathophysiological mechanisms that underlie levodopa- or dopamine agonist-induced dyskinesia in Parkinson’s disease: implications for future strategies in treatment. Mov Disord 1990;5:100-8. Narabayashi H, Yokochi F, Nakajima Y. Levodopa-induced dyskinesia and thalamotomy. J Neurol Neurosurg Psychiatr 1984;47:831-9. Backlund EO, Granberg PO, Hamberger B, Knutsson E, Martensson A, Sedvall G, Seiger A˚. Transplantation of adrenal medullary tissue to striatum in parkinsonism. First clinical trials. J Neurosurg 1985;62:169-73. Drucker-Colin R, Madrazo I, Diaz V. Open microsurgical autograft of adrenal medulla to caudate nucleus of patients with Parkinson’s disease. Schmitt Neurological Sciences Symposium, Rochester, NY, June 30–July 3, 1987. Madrazo I, Drucker-Colin R, Diaz V. Open microsurgical autograft of adrenal medulla to the right caudate nucleus in two patients with intractable Parkinson’s disease. N Engl J Med 1987;316:831-4. Bakay RA, Herring CJ. Central nervous system grafting in the treatment of parkinsonism. Stereotact Funct Neurosurg 1989;53:1-20.

History of stereotactic surgery

123. Goetz CG, De Long MR, Penn RD, Bakay RA. Neurosurgical horizons in Parkinson’s disease. Neurology 1993;43:1-7. 124. Hitchcock ER, Clough CG, Hughes RC, Kenny BG. Transplantation in Parkinson’s disease: stereotactic implantation of adrenal medulla and foetal mesencephalon. Acta Neurochir Suppl (Wien) 1989;46:48-50. 125. Stoddard SL, Ahlskog JE, Kelly PJ, Tyce GM, van Heerden JA, Zinsmeister AR, Carmichael SW. Decreased adrenal medullary catecholamines in adrenal transplanted parkinsonian patients compared to nephrectomy patients. Exp Neurol 1989;104:218-22. 126. Jankovic J, Grossman R, Goodman C, Pirozzolo F, Schneider L, Zhu Z, Scardino P, Garber AJ, Jhingran SG, Martin S. Clinical, biochemical, and neuropathologic findings following transplantation of adrenal medulla to the caudate nucleus for treatment of Parkinson’s disease. Neurology 1989;39:1227-34. 127. Gildenberg PL, Pettigrew LC, Merrell R, Butler I, Conklin R, Katz J, DeFrance J. Transplantation of adrenal medullary tissue to caudate nucleus using stereotactic techniques. Stereotact Funct Neurosurg 1990;54:268-71. 128. Mark VH, Gildenberg PL, Franklin PO (eds.). Proceedings of the colloquium on the use of embryonic cell transplantation for correction of CNS disorders. Appl Neurophysiol 1984;47:1-76. 129. Freed WJ, Cannon-Spoor HE, Krauthamer E. Intrastriatal adrenal medulla grafts in rats. Long-term survival and behavioral effects J Neurosurg 1986;65(5):664-70. 130. Bakay RA, Fiandaca MS, Barrow DL, Schiff A, Collins DC. Preliminary report on the use of fetal tissue transplantation to correct MPTP-induced Parkinson-like syndrome in primates. Appl Neurophysiol 1985;48:358-61. 131. Redmond DE, Jr, Roth RH, Spencer DD, Naftolin F, Leranth C, Robbins RJ, Marek KL, Elsworth JD, Taylor JR, Sass KJ. Neural transplantation for neurodegenerative diseases: past, present, and future. Ann NY Acad Sci 1993;695:258-66. 132. Lindvall O, Rehncrona S, Brundin P, Gustavii B, Astedt B, Widner H, Lindholm T, Bjorklund A, Tan M. Human fetal dopamine neurons grafted into the striatum in two patients with severe Parkinson’s disease. A detailed account of methodology and a 6-month followup. Arch Neurol 1989;46:615-31. 133. Bakay RA. Neurotransplantation: a clinical update. Acta Neurochir Suppl (Wien) 1993;58:8-16. 134. Breggin PR. The return of lobotomy and psychosurgery. Congressional Record 1972;118:24-6. 135. Spiegel EA, Wycis HT. Mesencephalotomy in intractable facial pain. Trans Am Neurol Assoc 1952;56:186-9. 136. Gybels JM, Sweet WH. Neurosurgical treatment of persistent pain. Pain and headache, vol. 11. Basel: Karger; 1989. 137. Gildenberg PL. History of pain management. In: Greenblatt SH, Dagi TF, editors. A history of neurosurgery. Park Ridge, IL: American Association of Neurological Surgeons; 1997. p. 465-88.

1

138. Trousseau A. De la ne´vralgie ´epileptiforme. Arch Gen Med 1853;1:33-44. 139. Rose W. Removal of the gasserian ganglion for severe neuralgia. Trans Med Soc Lond 1890;14:35-40. 140. Horsley V, Taylor J, Colman WS. Remarks on the various surgical procedures devised for the relief or cure of trigeminal neuralgia (tic douloureaux). Brit Med J 1891;2:1139-43. 141. Cushing H. A method for total extirpation of the Gasserian ganglion for trigeminal neuralgia. JAMA 1900;34:1035-41. 142. Cushing H. The major trigeminal neuralgias and their surgical treatment based on experiences with 332 Gasserian operations. I. Varieties of facial neuralgia. Am J Med Sci 1920;160:157-84. 143. Ramonede L. Exerese de trijumeau. Presse Med 1903;11:789-91. 144. Dandy WE. Section of the sensory root of the trigeminal nerve at the pons. Bull Johns Hopkins Hosp 1925;36:105-6. 145. Kirschner M. Zur Electrochirurgie. Arch Klin Chir 1931;161:761-8. 146. Kirschner M. Die Punktionstechnik u. Elektrokoagulation des Ganglion Gasseri. Arch Klin Chir 1933;176:581-620. 147. Murtagh F, Jr, Wycis HT, Spiegel EA. Relief of thalamic pain by mesencephalotomy. AMA Arch Neurol Psychiatry 1951;65:255-7. 148. Frazier CH. Section of the anterolateral columns of the spinal cord for the relief of pain. Arch Neurol Psychiatry 1920;4:137-47. 149. French LA. Cordotomy in the high cervical region for intractable pain. J Lancet 1953;73:283-7. 150. Spiller WG, Martin E. The treatment of persistent pain of organic origin in the lower part of the body by division of the anterolateral column of the spinal cord. J Am Med Assoc 1912;58:1489-90. 151. Gildenberg PL. Mesencephalotomy. In: Burchiel KJ, editor. Surgical management of pain. New York: Thieme; 2002. p. 786-94. 152. Iskandar BJ, Nashold BSJ. History of functional neurosurgery. Neurosurg Clin N Am 1995;6:1-25. 153. White JC, Sweet WH. Pain, its mechanism and neurosurgical control. Springfield, IL: Charles C Thomas; 1955. 154. Spiegel EA, Wycis HT, Szekely EG, Gildenberg PL. Medial and basal thalamotomy in so-called intractable pain. In: Knighton RS, Dumke PR, editors. Pain. Boston, MA: Little Brown; 1966. p. 503-17. 155. He´caen H, Talairach T, David M, Dell MB. Me´moires originaux. Coagulations limite´es du thalamus dans les algies du syndrome thalamique. Rev Neurol 1949;81:917-31. 156. Spiegel EA, Wycis HT. Mesencephalotomy in treatment of intractable facial pain. AMA Arch Neurol Psychiatry 1953;69:1-13.

29

30

1

History of stereotactic surgery

157. Spiegel EA, Wycis HT, Szekely EG, Gildenberg P, Zanes C. Combined dorsomedial, intralaminar and basal thalamotomy for relief of so-called intractable pain. J Int Coll Surg 1964;42:160-8. 158. Nashold BSJ, Wilson WP, Slaughter DG. Stereotaxic midbrain lesions for central dysesthesia and phantom pain. Preliminary report. J Neurosurg 1969; 30:116-26. 159. Nashold BS, Jr., Wilson WP, Slaughter DG. Sensations evoked by stimulation in the midbrain of man. J Neurosurg 1969;30:14-24. 160. Nashold BS, Jr. Extensive cephalic and oral pain relieved by midbrain tractotomy. Conf Neurol 1972;34:382-8. 161. Foltz EL, White LE, Jr. Pain ‘‘relief ’’ by frontal cingulumotomy. J Neurosurg 1962;19:89-100. 162. Mullan S, Moseley R, Harper PV. The creation of deep cerebral lesions by small beta ray sources implanted under guidance of fluoroscopic image intensifiers (as used in the treatment of Parkinson’s disease). Am J Roentgen 1959;82:613. 163. Mullan S, Harper PV, Hekmatpanah J, Torres H, Dobben G. Percutaneous interruption of spinal pain tracts by means of a strontium-90 needle. J Neurosurg 1963;20:931-9. 164. Rosomoff HL, Carrol F, Brown J, Sheptak P. Percutaneous radiofrequency cervical cordotomy: technique. J Neurosurg 1965;23:639-44. 165. Tenicela R, Rosomoff HL, Feist J, Safar P. Pulmonary function following percutaneous cervical cordotomy. Anesthesiology 1968;29:7-16. 166. Lin PM, Gildenberg PL, Polakoff PP. An anterior approach to percutaneous lower cervical cordotomy. J Neurosurg 1966;25:553-60. 167. Sjo¨qvist O. Eine neue Operationsmethode bei Trigeminusneuralgie: durchschneidung des Tractus spinalis trigemini. Zentralbl f Neurochir 1937;2:274-81. 168. White JC, Sweet WH. Pain and the neurosurgeon. A forty year experience. Springfield, IL: Charles C Thomas; 1969. 169. Hitchcock E. Stereotactic trigeminal tractotomy. Farmatsiia 1970;19:131-5. 170. Hitchcock E. Stereotactic cervical myelotomy. J Neurol Neurosurg Psychiatry 1970;33:224-30. 171. Crue BL, Todd EM, Carregal EJA. Posterior approach for high cervical percutaneous radiofrequency cordotomy. Confinia Neurol 1968;30:41-52. 172. Gildenberg PL. Evolution of spinal cord surgery for pain. Clin Neurosurg 2006;53:11-17. 173. Hitchcock E. Stereotactic myelotomy. Proc R Soc Med 1974;67:771-2. 174. Schvarcz JR. Stereotactic extralemniscal myelotomy. J Neurol Neurosurg Psychiatry 1976;39:53-7. 175. Gildenberg PL, Hirshberg RM. Limited myelotomy for the treatment of intractable cancer pain. J Neurol Neurosurg Psychiatry 1984;47:94-6.

176. Stillings D. The first use of electricity for pain treatment. Medtronic Archive on Electro-Stimulation 1971. 177. Isaacson W. Benjamin Franklin. An American life. New York: Simon & Schuster; 2003. 178. Pruel MC. A history of neuroscience from Galen to Gall. In: Greenblatt SH, Dagi TF, Epstein MH, editors. A history of neurosurgery. Park Ridge, IL: American Association of Neurological Surgeons; 1997. p. 99-130. 179. Shelly M. Frankenstein. Oxford: Oxford Press; 1818. ¨ ber die elektrische Erregbarkeit 180. Fritsch G, Hitzig E. U des Grosshirns. Arch Anat Physiol wiss Med 1870;37:300-32. 181. Morgan JP. The first reported case of electrical stimulation of the human brain. J Hist Med Allied Sci 1982;37:51-64. 182. Vilensky JA, Gilman S. Horsley was the first to use electrical stimulation of the human cerebral cortex intraoperatively. Surg Neurol 2002;58:425-6. 183. Hassler R, Riechert T, Mundinger F, Umbach W, Ganglberger JA. Physiological observations in stereotaxic operations in extrapyramidal motor disturbances. Brain 1960;83:337-50. 184. Tasker RR, Organ LW, Hawrylshyn PA. The thalamus and midbrain of man. A physiological atlas using electrical stimulation. Springfield, IL: Charles C Thomas; 1982. 185. Woolsey CN. Cortical localization as defined by evoked potential and electrical stimulation studies. In: Schaltenbrand G, Woolsey CN, editors. Cerebral localization and organization. Madison, WI: University of Wisconsin Press; 1964. p. 17-26. 186. Pool JL. Psychosurgery in older people. J Am Geriatr Soc 1954;2:456-65. 187. Heath RG. Exploring the mind-brain relationship. Baton Rouge, LA: Moran Printing, Inc.; 1996. 188. Olds J, Milner P. Positive reinforcement produced by electrical stimulation of the septal area and other regions of the rat brain. J Comp Physiol Psychol 1954;47:419-27. 189. Heath RG. Psychiatry. Annu Rev Med 1954;5:223-36. 190. Gol A. Relief of pain by electrical stimulation of the septal area. J Neurol Sci 1967;5:115-20. 191. Bechtereva NP, Bondarchuk AN, Smirnov VM. Therapeutic electrostimulations of the deep brain structures. Vopr Neirokhir 1972;1:7-12. 192. Melzack R, Wall PD. Pain mechanisms: a new theory. Science 1965;150:971-9. 193. Laitinen L. Placement of electrodes in transcutaneous stimulation for chronic pain. Neurochirurgie 1976; 22:517-26. 194. Wall PD, Sweet WH. Temporary abolition of pain in man. Science 1967;155:108-9. 195. Sweet WH, Wepsic JG. Treatment of chronic pain by stimulation of fibers of primary afferent neuron. Trans Am Neurol Assoc 1968;93:103-7.

History of stereotactic surgery

196. Shealy CN, Mortimer JT, Reswick JB. Electrical inhibition of pain by stimulation of the dorsal columns. Preliminary clinical report. Anesth Analg (Cleve) 1967;46:489-91. 197. Gildenberg PL. Treatment of spasmodic torticollis with dorsal column stimulation. Acta Neurochir (Wien) 1977;24:Suppl65-6. 198. Cook AW. Electrical stimulation in multiple sclerosis. Hosp Pract 1976;11:51-8. 199. Dooley DM. Spinal cord stimulation. AORN J 1976;23:1209-12. 200. Dooley DM, Kasprak M. Modification of blood flow to the extremities by electrical stimulation of the nervous system. South Med J 1976;69:1309-11. 201. Hosobuchi Y, Adams JE, Rutkins B. Chronic thalamic stimulation for the control of facial anesthesia dolorosas. Arch Neurol 1973;29:158-61. 202. Mundinger F. New stereotactic treatment of spasmodic torticollis with a brain stimulation system (author’s transl). Med Klin 1977;72:1982-6. 203. Reynolds DV. Surgery in the rat during electrical analgesia induced by focal brain stimulation. Science 1969;164:444-5. 204. Richardson DE, Akil H. Pain reduction by electrical brain stimulation in man. Part 1: Acute administration in periaqueductal and periventricular sites. J Neurosurg 1977;47:178-83. 205. Gildenberg PL. Symposium on the safety and clinical efficacy of implanted neuroaugmentive devices. Appl Neurophysiol 1977;40:69-240. 206. Tsubokawa T, Katayama Y, Yamamoto T, Hirayama T, Koyama S. Chronic motor cortex stimulation for the treatment of central pain. Acta Neurochir Suppl (Wien) 1991;52:137-9. 207. Migita K, Uozumi T, Arita K, Monden S. Transcranial magnetic coil stimulation of motor cortex in patients with central pain. Neurosurgery 1995;36:1037-9. 208. Gildenberg PL. History of neuroaugmentative procedures for chronic pain. Neurosurg Clin N Am 2003;14:327-37. 209. Gildenberg PL. History of electrical neuromodulation for chronic pain. Pain Med 2006;7Suppl 1:S7-13. 210. Gildenberg PL. The use of pacemakers (electrical stimulation) in functional neurological disorders. In: Rasmussen T, Marino R, editors. Functional neurosurgery. New York: Raven Press; 1979. p. 59-74. 211. Laitinen LV, Bergenheim AT, Hariz MI. Ventroposterolateral pallidotomy can abolish all parkinsonian symptoms. Stereotact Funct Neurosurg 1992;58:14-21. 212. Spiegel EA, Wycis HT. Ansotomy in paralysis agitans. AMA Arch Neurol Psychiatry 1953;69:652-3. 213. Goetz CG, Diederich NJ. There is a renaissance of interest in pallidotomy for Parkinson’s disease. Nat Med 1996;2:510-4. 214. Iacono RP, Shima F, Lonser RR, Kuniyoshi S, Maeda G, Yamada S. The results, indications, and physiology of

215.

216.

217.

218.

219.

220.

221.

222.

223.

224.

225.

226.

1

posteroventral pallidotomy for patients with Parkinson’s disease. Neurosurgery 1995;36:1118-27. Favre J, Taha JM, Nguyen TT, Gildenberg PL, Burchiel KJ. Pallidotomy: a survey of current practice in North America. Neurosurgery 1996;39:883-92. Lozano A, Hutchison W, Kiss Z, Tasker R, Davis K, Dostrovsky J. Methods for microelectrode-guided posteroventral pallidotomy. J Neurosurg 1996;84: 194-202. Krauss JK, Grossman RG. Historical review of pallidal surgery for treatment of parkinsonism and other movement disorders. In: Krauss JK, Grossman RG, Jankovic J, editors. Pallidal surgery for the treatment of Parkinson’s disease and movement disorders. Philadelphia, PA: Lippincott-Raven; 1998. p. 1-23. Vitek JL, Bakay RA. The role of pallidotomy in Parkinson’s disease and dystonia. Curr Opin Neurol 1997;10:332-9. Nandi D, Chir M, Liu X, Bain P, Parkin S, Joint C, Winter J, Stein J, Scott R, Gregory R, Aziz T. Electrophysiological confirmation of the zona incerta as a target for surgical treatment of disabling involuntary arm movements in multiple sclerosis: use of local field potentials. J Clin Neurosci 2002;9:64-8. Meier MJ, Story J, French LA, Chou SN. Quantitative assessment of behavioral changes following subthalamotomy in the treatment of Parkinson’s disease. Confin Neurol 1966;27:154-61. Brice J, McLellan L. Suppression of intention tremor by contingent deep-brain stimulation. Lancet 1980; 1:1221-2. Benabid AL, Pollak P, Gervason C, Hoffmann D, Gao DM, Hommel M, Perret JE, de Rougemont J. Longterm suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 1991;337:403-6. Siegfried J, Lippitz B. Chronic electrical stimulation of the VL-VPL complex and of the pallidum in the treatment of movement disorders: personal experience since 1982. Stereotact Funct Neurosurg 1994; 62:71-5. Benabid AL, Pollak P, Gross C, Hoffmann D, Benazzouz A, Gao DM, Laurent A, Gentil M, Perret J. Acute and long-term effects of subthalamic nucleus stimulation in Parkinson’s disease. Stereotact Funct Neurosurg 1994;62:76-84. Alvarez L, Macias R, Guridi J, Lopez G, Alvarez E, Maragoto C, Teijeiro J, Torres A, Pavon N, Rodriguez-Oroz MC, Ochoa L, Hetherington H, Juncos J, Delong MR, Obeso JA. Dorsal subthalamotomy for Parkinson’s disease. Mov Disord 2001;16:72-8. Jimenez F, Velasco F, Velasco M, Brito F, Morel C, Marquez I, Perez ML. Subthalamic prelemniscal radiation stimulation for the treatment of Parkinson’s disease: electrophysiological characterization of the area. Arch Med Res 2000;31:270-81.

31

32

1

History of stereotactic surgery

227. Spiegel EA, Wycis HT, Szekely EG, Adams DJ, Flanagan M, Baird HW, III. Campotomy in various extrapyramidal disorders. J Neurosurg 1963;20:871-84. 228. Gildenberg PL. Evolution of neuromodulation. Stereotact Funct Neurosurg 2005;83:71-9. 229. Krauss JK, Pohle T, Weber S, Ozdoba C, Burgunder JM. Bilateral stimulation of globus pallidus internus for treatment of cervical dystonia. Lancet 1999; 354:837-8. 230. Coubes P, Roubertie A, Vayssiere N, Hemm S, Echenne B. Treatment of DYT1-generalised dystonia by stimulation of the internal globus pallidus. Lancet 2000;355:2220-1. 231. Kumar R, Dagher A, Hutchison WD, Lang AE, Lozano AM. Globus pallidus deep brain stimulation for generalized dystonia: clinical and PET investigation. Neurology 1999;53:871-4. ¨ ber einen Fall von doppelseitiger 232. Hassler R, Riechert T. U Fornicotomie bei sogenannter temporaler Epilepsie. Acta Neurochir (Wien) 1957;5:330-40. 233. Pagni CA. Stereo-electroencephalographic observations on the psychomotor seizure. Confin Neurol 1966; 27:137-43. 234. Umbach W, Riechert T. The stereotactic coagulation of the fornix as treatment of temporal lobe epilepsy. Proc First Int Congress Neurol Sci 1961;3:565-78. 235. Jinnai D, Nishimoto A. Stereotaxic destruction of Forel H for treatment of epilepsy. Neurochirurgia(Stuttgart) 1963;6:164-76. 236. Laitinen L. Thalmotomy in progressive myoclonus epilepsy. Acta Neurol Scand 1967;43:31-47. 237. Umbach W. Long-term results of fornicotomy for temporal epilepsy. Confin Neurol 1966;27:121-3. 238. Munari C, Hoffmann D, Francione S, Kahane P, Tassi L, Lo Russo G, Benabid AL. Stereo-electroencephalography methodology: advantages and limits. Acta Neurol Scand Suppl 1968;152:56-67. 239. Mundinger F, Becker P, Groebner E, Bachschmid G. Late results of stereotactic surgery of epilepsy predominantly temporal lobetype. Acta Neurochir (Wien) 1976;23Suppl:177-82. 240. Nashold BS, Jr, Flanigin H, Jr, Wilson WP, Stewart B. Stereotactic evaluation of bitemporal epilepsy with electrodes and lesions. Confin Neurol 1973; 35:94-100. 241. Vaernet K. Stereotaxic amygdalotomy in temporal lobe epilepsy. Confin Neurol 1972;34:176-80. 242. Olivier A, Gloor P, Andermann F, Quesney LF. The place of stereotactic depth electrode recording in epilepsy. Appl Neurophysiol 1985;48:395-9. 243. Gildenberg PL. Unpublished data. 1990. 244. Fins JJ. From psychosurgery to neuromodulation and palliation: history’s lessons for the ethical conduct and regulation of neuropsychiatric research. Neurosurg Clin N Am 2003;14:303-6. 245. Spiegel EA, Wycis HT. The central mechanism of emotions. Am J Psychiatry 1951;109:426-31.

246. Orchinik C, Koch R, Wycis HT, Freed H, Spiegel EA. The effect of thalamic lesions upon the emotional reactivity (Rorschach and behavior studies). Res Publ Assoc Res Nerv Ment Dis 1949;29:172-207. 247. Sano K. Sedative neurosurgery with special reference to posteromedial hypothalamotomy. Neurol Med Chir (Tokyo) 1962;4:112. 248. Spiegel EA, Wycis HT, Freed H, Orchinik C. The central mechanism of the emotions; (experiences with circumscribed thalamic lesions). Am J Psychiatry 1951;108:426-32. 249. Gildenberg PL (ed.). Functional neurosurgery. Neurosurg Clin N Am 1995;6:1-181. 250. Fodstad H, Strandman E, Karlsson B, West KA. Treatment of chronic obsessive compulsive states with stereotactic anterior capsulotomy or cingulotomy. Acta Neurochir (Wien) 1982;62:1-23. 251. Martuza RL, Chiocca EA, Jenike MA, Giriunas IE, Ballantine HT. Stereotactic radiofrequency thermal cingulotomy for obsessive compulsive disorder. J Neuropsychiatry Clin Neurosci 1990;2:331-6. 252. Andy OJ, Jurko F. Thalamic stimulation effects on reactive depression. Appl Neurophysiol 1987;50:324-9. 253. Diering SL, Bell WO. Functional neurosurgery for psychiatric disorders: a historical perspective. Stereotact Funct Neurosurg 1991;57:175-94. 254. Benabid AL, Wallace B, Mitrofanis J, Xia R, Piallat B, Chabardes S, Berger F. A putative generalized model of the effects and mechanism of action of high frequency electrical stimulation of the central nervous system. Acta Neurol Belg 2005;105:149-57. 255. Kopell BH, Greenberg B, Rezai AR. Deep brain stimulation for psychiatric disorders. J Clin Neurophysiol 2004;21:51-67. 256. Lienhard JH. Inventing modern. Oxford Press; Oxford: 257. Murtagh F, Wycis HT, Robbins R, Spiegel-Adolph M, Spiegel EA. Visualization and treatment of cystic brain tumors by stereoencephalotomy. Acta Radiol 1956;46:407-14. 258. Gildenberg PL, Kaufman HH. Direct calculation of stereotactic coordinates from CT scans. Appl Neurophysiol 1982;45:347-51. 259. Gildenberg PL, Kaufman HH, Murthy KS. Calculation of stereotactic coordinates from the computed tomographic scan. Neurosurgery 1982;10:580-6. 260. Gildenberg PL. Computerized tomography and stereotactic surgery. In: Spiegel EA, editor. Guided brain operations. Basel: Karger; 1982. p. 24-34. 261. Leksell L, Jernberg B. Stereotaxis and tomography: a technical note with six figures. Acta Neurochir 1980;52:1-7. 262. Barcia-Salorio JL, Broseta J, Hernandez G, Roldan P, Bordes V. A new approach for directed CT localization in stereotaxis. Appl Neurophysiol 1982;45:383-6. 263. Colombo F, Angrilli F, Zanardo A, Pinna V, Alexandre A, Benedetti A. A universal method to employ

History of stereotactic surgery

264.

265. 266.

267. 268.

269.

270.

271.

272.

273.

274.

275. 276. 277.

278.

279.

280.

CT scanner spatial information in stereotactic surgery. Appl Neurophysiol 1982;45:352-65. Colombo F, Angrilli F, Zanardo A, Pinna V, Benedetti A. A new method for utilizing CT data in stereotactic surgery: measurement and transformation technique. Acta Neurochir (Wien) 1981;57: 195-203. Patil AA. Compute tomography-oriented stereotactic system. Neurosurgery 1982;10:370-4. Koslow M, Abele MG. A fully interfaced computerized tomographic-stereotactic surgical system. Appl Neurophysiol 1980;43:174-5. Lunsford LD. A dedicated CT system for the stereotactic operating room. Appl Neurophysiol 1982;45:374-8. Brown RA, Roberts TS, Osborn AG. Stereotaxic frame and computer software for CT-directed neurosurgical localization. Invest Radiol 1980;15:308-12. Kelly PJ, Kall B, Goerss S, Alker GJ, Jr. Precision resection of intra-axial CNS lesions by CT-based stereotactic craniotomy and computer monitored CO2 laser. Acta Neurochir (Wien) 1983;68:1-9. Leksell L, Leksell D, Schwebel J. Stereotaxis and nuclear magnetic resonance. J Neurol Neurosurg Psychiatry 1985;48:14-18. Broggi G, Franzini A, Peluchetti D, Servello D. Treatment of deep brain abscesses by stereotactic implantation of an intracavitary device for evacuation and local application of antibiotics. Acta Neurochir (Wien) 1985;76:94-8. Backlund EO, von Holst H. Controlled subtotal evacuation of intracerebral haematomas by stereotactic technique. Surg Neurol 1978;9:99-101. Tanikawa T, Amano K, Kawamura H, Kawabatake H, Notani M, Iseki H, Shiwaku T, Nagao T, Iwata Y, Taira T. CT-guided stereotactic surgery for evacuation of hypertensive intracerebral hematoma. Appl Neurophysiol 1985;48:431-9. Zamorano L, Chavantes C, Dujovny M, Malik G, Ausman J. Stereotactic endoscopic interventions in cystic and intraventricular brain lesions. Acta Neurochir Suppl (Wien) 1992;54:69-76. Gildenberg PL, Labuz J. Use of a volumetric target for image-guided surgery. Neurosurgery 2006;59:651-9. Bernstein M, Gutin PH. Interstitial irradiation of brain tumors: a review. Neurosurgery 1981;9:741-50. Gildenberg PL, Woo S, Butler B, Grant W, Berner B. Fractionated brachytherapy: catheter insertion and dosimetry. Stereotact Funct Neurosurg 1994;63:246-9. Kelly PJ, Alker GJ, Jr. A method for stereotactic laser microsurgery in the treatment of deep seated CNS neoplasms. Appl Neurophysiol 1980;43:210-5. Kall BA, Kelly PJ, Goerss SJ. Interactive stereotactic surgical system for the removal of intracranial tumors utilizing the CO2 laser and CT-derived database. IEEE Trans Biomed Eng 1985;32:112-6. Kelly PJ. Tumor stereotaxis. Philadelphia, PA: Saunders; 1991.

1

281. Kelly PJ, Kall BA, Goerss S. Transposition of volumetric information derived from computed tomography scanning into stereotactic space. Surg Neurol 1984; 21:465-71. 282. Kosugi Y, Watanabe E, Goto J, Watanabe T, Yoshimoto S, Takakura K, Ikebe J. An articulated neurosurgical navigation system using MRI and CT images. IEEE Trans Biomed Eng 1988;35:147-52. 283. Roberts DW, Strohbehn JW, Hatch JF, Murray W, Kettenberger H. A frameless stereotaxic integration of computerized tomographic imaging and the operating microscope. J Neurosurg 1986;65:545-9. 284. Rousu JS, Kohls PE, Kall B, Kelly PJ. Computer-assisted image-guided surgery using the regulus navigator. Stud Health Technol Inform 1998;50:103-9. 285. Heilbrun MP, McDonald P, Wiker C, Koehler S, Peters W. Stereotactic localization and guidance using a machine vision technique. Stereotact Funct Neurosurg 1992;58:94-8. 286. Day R, Heilbrun MP, Koehler S, McDonald P, Peters W, Siemionow V. Three-point transformation for integration of multiple coordinate systems: applications to tumor, functional, and fractionated radiosurgery stereotactic planning. Stereotact Funct Neurosurg 1994;63:76-9. 287. Heilbrun MP, Koehler S, MacDonald P, Siemionow V, Peters W. Preliminary experience using an optimized three-point transformation algorithm for spatial registration of coordinate systems: a method of noninvasive localization using frame-based stereotactic guidance systems. J Neurosurg 1994;81:676-82. 288. Smith KR, Frank KJ, Bucholz RD. The NeuroStation – a highly accurate, minimally invasive solution to frameless stereotactic neurosurgery. Comput Med Imag Graphics 1994;18:247-56. 289. Gildenberg PL. The Exoscope system for three-dimensional craniotomy. In: Gildenberg PL, Tasker RR, editors. Textbook of stereotactic and functional neurosurgery. New York: Mc-Graw-Hill; 1997. p. 485-90. 290. Gildenberg PL, Ledoux R, Cosman E, Labuz J. The Exoscope – a frame-based video/graphics system for intraoperative guidance of surgical resection. Stereotact Funct Neurosurg 1994;63:23-5. 291. Zamorano L, Dujovny M, Chavantes C, Malik G, Ausman J. Image-guided stereotactic centered craniotomy and laser resection of solid intracranial lesions. Stereotact Funct Neurosurg 1990;54/55:398-403. 292. Gildenberg PL, Labuz J. Stereotactic craniotomy with the exoscope. Stereotact Funct Neurosurg 1997;68:64-71. 293. Pillay PK, Gildenberg PL, Labuz J. Computer workstation applications: stereoplan, virtual reality, and the Gildenberg exoscope. In: Pell MF, Thomas DGT, editors. Handbook of stereotaxy using the CRW apparatus. Baltimore, MD: Williams & Wilkins; 1994. p. 219-33. 294. Gildenberg PL. Confinia neurologica/applied neurophysiology. 50 years. Appl Neurophysiol 1988;51:1-5.

33

11 History of Stereotactic Surgery in China F.-C. Lee . B. Sun . J. Zhang . K. Zhang . F.-G. Meng

Prehistoric and Feudal China China is unique among the world civilizations in that it has a well-established indigenous medical treatment philosophy dating back thousands of years. This was epitomized by the well known Huang Ti Nei Jing (Yellow Emperor’s Inner Classic), a seminal medical text of ancient China where a legendary physician Yu Fu was alleged to possess the skill for surgical exposure of the brain. The Neijing, Shennong Ben Cao Jing (Divine Husbandman’s Classic of the Materia Medica), and a few other ancient texts laid the foundation of the so-called Traditional Chinese Medicine (TCM), an alternative treatment being actively practiced even today in mainland China and among overseas Chinese alongside modern Western medical and surgical therapies. A good depiction appeared in the popular History of the Three Kingdoms where ‘‘cranial surgery’’ was proposed by Hua Tuo (Hua Lun), a famous physician, on one of the three reigning kings Cao Cao who suffered persistent headaches, presumably due to battle trauma–related intracranial hematoma (or perhaps even intracranial tumor) during the turbulent warring period of Eastern Han and Three Kingdoms (222–280 A.D.). Hua Tuo (> Figure 11‐1) had also reportedly performed surgeries with anesthesia, 1,600 years ahead of similar endeavors in Western Civilization, using wine and a herbal concoction of cannabis boil powder. Incidentally, Hua Tuo came from the ancient Qiao City of Pei State in the modern day Anhui Province, where China’s first

#

Springer-Verlag Berlin/Heidelberg 2009

stereotactic neurosurgery institute and training center was established in 1983 and the first National Stereotactic and Functional Neurosurgical Conference was held on June 8–14, 1987. The oldest prehistoric evidence of human trephination in European Civilization was probably the Ensisheim Stone Age skull unearthed from a burial site in France which was dated to 5100 B.C. [1]. Archaeological evidence also surfaced in China in 1995 with the excavation in Shandong Province of an adult male skull, aged 35–45 years, bearing a 31  25 mm round parietal calvarial defect with smooth border. The perimeter showed evidence of scrapping and bone regeneration. This belonged to an ancient inhabitant of the Dawen Kou Culture (third to fifth millennium B.C.) and was 14C-dated to about 5000 B.C. (> Figure 11‐2). The opening appeared to have been made with tools resembling a trephine. This lends credence to the conclusion that trephinations were probably performed in Neolithic China. Similar finds were discovered at other archaeological sites in the Qinghai, Heilongjiang, and Henan Provinces of China, variously radiocarbon-dated to between 2000 and 4000 B.C. [2]. The motivation for these skull openings remained varied and speculative, just like in other European archaeological discoveries of the Paleolithic and Neolithic period. Whether for curative or ritual purposes to heal and alter behavior, these could have been early men’s attempt to relate structure to functions and behavior, perhaps a primitive version of modern day functional neurosurgery.

126

11

History of stereotactic surgery in china

Birth of Neurosurgery in Modern China An understanding of the development of stereotactic and functional neurosurgery in China will . Figure 11‐1 Hua Tuo (Hua Lun), born 208 B.C. in Qiao (present Anhui Province, China)

be incomplete without due reference to the history of general neurosurgery, the foundation on which the former has evolved. Modern neurosurgery did not develop much until the last century of Chinese history. Like the rest of the Chinese civilization, it was shrouded in mystery behind the ‘‘bamboo curtain’’ as a result of the cultural and diplomatic isolation of this monolithic, inward-looking nation. The country was plagued by the ineffective, feudalistic Imperial Manchurian rule, subsequently overthrown in 1912 in a popular revolution led by Dr Sun Yat-sen, the father and founder of modern China. Due credit should be given to Dr Song-Tao Guan (ST Kuan) and Dr Cha-Li Zhang (Charles Chang) from Beijing and Shenyang, respectively, for their pioneering works in neurosurgery in China [3]. Guan completed his residency program at the Peking Union Medical College Hospital (PUMC) in 1926. PUMC was jointly founded in 1906 by the American Board of Commissioner for Foreign Missions, the Presbyterian Church in the USA, the Methodist Episcopal Church, and the London Missionary Society, among others. From 1926 to1930 Guan received neurosurgery training at the University of

. Figure 11‐2 Archaeological find at Dawen Kou 5000 B.C. (picture courtesy of Cheng-Yuan Wu)

History of stereotactic surgery in china

Pennsylvania under Dr Charles H. Frazier, who was among the first group of American neurosurgeons who established neurosurgery as a new discipline from general surgery. In 1938 Yi-Cheng Zhao, another graduate from the same medical college, was sent by the Rockefeller Foundation (established 1913), through its subsidiary, the China Medical Board, for formal neurosurgical training under Dr Wilder Penfield at the Montreal Neurological Institute at McGill University. Upon his return to China in 1940, Zhao practiced neurosurgery at the PUMC Hospital with Guan. In 1952, three years after the Chinese civil war ended with the establishment of the People’s Republic of China, Zhao founded the first Brain Department comprising neurology and neurosurgery in the port city of Tianjin, one of the very few cities with early Western influence in the ethnophobic China of the nineteenth century. It was reluctantly opened by the Qing Dynasty of China as a treaty port accessible to France, Britain, and others in 1860. Formal concessions with foreign settlements were ceded to Western powers and Japan in 1903 after the Imperial Qing Dynasty’s defeat in the war during the Boxer Rebellion of 1899. These three neurosurgeons, along with Tong-He Zhang of Xian City, performed the first neurosurgical procedures in modern China. Zhang performed prefrontal lobotomy for a psychiatric disorder [4]. From 1932 to 1949, only 16 neurosurgical articles were published in the indigenous Chinese Medical Journal (CMJ), which was initially established in 1887 in Shanghai as China Medical Missionary Journal for publications mainly by Western medical missionaries serving in China. The name was changed to China Medical Journal in 1907, thereafter adopted its current name of CMJ in 1932, when it merged with the English language section of National Medical Journal of China. Only about 60 brain tumors were reported in the Chinese literature. With his training under Dr Frazier who pioneered subtemporal retrogasserian neurotomy in

11

1910 as a permanent cure for tic douloureux, Guan reported his experience with Frazier’s operation for trigeminal neuralgia in 1932 in the CMJ [5]. Charles Chang published on similar procedure and alcohol block three years after Guan. He also drew attention to the occurrence of anesthesia dolorosa and abducens nerve palsy and reported on neurofibroma of the Gasserian ganglion [6]. However, further progress in the development of neurosurgery was repeatedly halted when the country was plunged into two devastating civil wars between the ruling Nationalist Army (Kuomintang) and the Communist People’s Liberation Army (PLA) from 1927 to 1936 and 1946 to 1949, with an intervening period of brutal invasion of China by the Japanese Imperial Army that lasted from 1937 to 1945 when World War II finally ended (> Figure 11‐3). Before the formation of the communist People’s Republic of China (PRC) in 1949, international assistance in the development of neurosurgery as in many other fields was predominantly rendered by the United States and European nations mainly through the China Medical Board. After 1949, however, international collaborations were confined to fellow Communist Bloc countries, in particular the USSR. A 6 month neurosurgery training course was conducted in Beijing by Dr A.E. Arutiunov from the Kiev Neurosurgical Institute of the former Soviet Union in October 1954. Participants of this program included Chung-Cheng Wang (Zhong-Cheng Wang), Ya-Du Zhao, and Da-Jie Jiang, while others were sent to the prestigious Moscow Burdenko Neurosurgical Institute. Among them, Tong-Jin Tu set up a neurosurgery service for the People’s Liberation Army in the Fourth Military Medical University in Xian City (ancient capital of Qin dynasty 221–206 B.C.) upon his return to China in 1956. The T J Tu Award for excellence in neurosurgery was established in honor of his invaluable contributions to military neurosurgery. DrYi-Cheng Zhao (> Figure 11‐4) founded the first Brain Department in China, comprising

127

128

11

History of stereotactic surgery in china

. Figure 11‐3 Some early Chinese textbooks, journals, and monographs on stereotactic and functional neurosurgery

. Figure 11‐4 Dr Yi-Cheng Zhao (1908–1974), Father of Neurosurgery of China

neurology and neurosurgery services at the Tianjin Municipal General Hospital in 1952 aided by his students Chung-Cheng Wang and Qing-Cheng Xu. The Neurosurgery Department

at the Beijing Tong-Ren Hospital was established two years later. It was later shifted to the XuanWu Hospital, the predecessor of the Beijing Neurosurgical Institute, the largest neurological center in China. A one-year intensive formal postgraduate neurosurgery training program was started in Tianjin in 1953. The graduates from these programs were to form the core group and foundation of modern neurosurgery in China. Dr Zhao established the Beijing Neurosurgical Institute in March 1960, holding the position of director until his untimely demise in1974, whereupon his student Chung-Cheng Wang took over. The Beijing Neurosurgical Institute, which is now housed within the Beijing Tiantan Hospital, is currently the national clinical, research, and training center with over 300 neurosurgical beds divided into craniocerebral injury, cerebrovascular disease, spinal injury, skull base surgery, intracranial tumors, pediatric neurosurgery, stereotactic and functional neurosurgery, and neurointensive care units in addition to ten research departments. Its basic neuroscience research departments cover neuroanatomy, neurotransmitter, neuropathology, neuropharmacology, neuroepidemiology,

History of stereotactic surgery in china

cytobiology, neurophysiology, immunology, neurochemistry, and electron microscopy. The faculty is led by prominent neurosurgeons like Chung-Cheng Wang, Ya-Do Zhao, Shi-Qi Luo, and Ji-Zong Zhao. More than 1000 neurosurgeons have benefited from its training programs till date. Further south in Shanghai, yet another city subjected to early Western influence after the Opium War with Britain in 1840–1843, neurosurgery service was established in 1953 in the Shanghai Red Cross Society Hospital, the predecessor of the Shanghai Huashan Hospital, by Yu-Quan Shi and Zhen-Qin Zhu. This prestigious institution has been credited with the first Chinese-made stereotactic frame and the first indigenously designed operating microscope and pioneered hemispherectomy for infantile hemiplegia in 1959. Postgraduate neurosurgery training programs have been offered since 1958. Shi retired from the Chair of the Department of Neurosurgery in 1989. The Shanghai Huashan Hospital was incorporated into the Shanghai Huashan Institute of Neurological Surgery (SHIN) in March 2000, with a total annual operative statistics exceeding 4,000. After the inception of the PRC in 1949, there were periodic sociopolitical upheavals, in particular the notorious Chinese Cultural Revolution from 1966 to 1976, causing widespread social, political, and economic chaos throughout the country. Scholastic aptitude was considered bourgeois and decadent and could constitute the basis for severe persecution. Not surprisingly, there was a striking absence of neurosurgical publications during this ‘‘Dark Age’’ of modern Chinese history. Until the beginning of the long anticipated economic reform in 1978 by leader Deng XiaoPing, the country endured diplomatic and cultural isolation, compounded further by economic embargo from Western nations due to ideological difference, a legacy of the Cold War. Language barrier and paucity in resources meant that innovative Chinese neurosurgeons had to develop

11

skills de novo and design diagnostic and surgical equipment, often under conditions harsh by Western standards. Their works have been documented in monographs and native Chinese journals such as the Chinese Medical Journal, Chinese Journal of Neurosurgery, Chinese Clinical Neurosurgery, and subspecialty journals, e.g., Chinese Journal of Stereotactic and Functional Neurosurgery, and Chinese Journal of Minimally Invasive Neurosurgery. It is only perhaps in the last decade or so that more and more Chinese neurosurgeons armed with better command of foreign languages have made their works known to the rest of the world through international journals such as Journal of Neurosurgery, Neurosurgery, British Journal of Neurosurgery, Stereotactic and Functional Neurosurgery, etc. (> Figure 11‐5). . Figure 11‐5 The first issue of the Chinese Journal of Stereotactic and Functional Neurosurgery (published in Anhui Province, China, 1986)

129

130

11

History of stereotactic surgery in china

Stereotactic and Functioning Neurosurgery Historical Developments in China In the 1940s, psychosurgery was reportedly being carried out by Dr T.H. Zhang. Stereotactic neurosurgery has advanced with strides in North America and Europe since 1946 when SpiegelWycis performed the first human stereotactic pallidotomy [7,8] and Prof. Lars Leksell invented of the Leksell stereotactic frame using polar coordinates in 1949 [9]. Nevertheless, the first surgical treatment for Parkinson’s disease in China was a freehand transorbital pallidotomy using Novocain and Iodipamide by Chung-Cheng Wang in 1959 [10]. Chung-Cheng Wang and fellow contemporaries Jian-Pin Xu, Mao-Shan Wang, and Da-Jie Jiang were the forerunners of stereotactic and functional neurosurgery in China.

In 1963, Dr Jian-Ping Xu, currently in the Guangdong Hospital of Traditional Chinese Medicine, completed a two-year training at the Moscow Neurosurgical Institute under the tutelage of Dr Edvard I. Kandel, who was the first Soviet neurosurgeon trained in stereotactic surgery. In the same year, Xu embarked on stereotactic surgery on patients with Parkinson’s disease using his self-designed Cartesian coordinates–based stereotactic frame in Anhui [11]. Sheer necessity and lack of recourse to expensive Western products motivated many Chinese surgeons, notably MaoShan Wang and Da-Jie Jiang of the Shanghai Medical University, in the early 1960s to design stereotactic devices to be used in, e.g., pallidotomy and thalamotomy for extrapyramidal disease [12–14]. Da-Jie Jiang’s frame (> Figure 11‐6 left) was an attempt to incorporate features of the two main groups of stereotactic devices available in the West then. Devices in the first category were

. Figure 11‐6 Stereotactic head frame designed by Da-Jie Jiang, Shanghai, 1964 (left) and with Li Pan 1989 (right) (with permission)

History of stereotactic surgery in china

structurally and mathematically complex, bulky, and difficult to operate. Specialized X-rays were needed. However, they offered a high degree of accuracy. These were exemplified by the SpiegelWycis, Leksell, Riechert, and Talairach equipment [7,9,15,16]. The second was represented by the Cooper and Austin devices [17,18]. These were structurally simple and easy to use but were compromised by a lower degree of accuracy even with repeated intraoperative adjustments with X-rays. Complications were also more prevalent. Limitations in target precision, control of lesion size, and higher degree of complications resulted in the waning of enthusiasm for these early stereotactic procedures (> Figure 11‐7). During the first decade of Western stereotactic neurosurgery, surgeons designed and custom-made their own stereotactic apparatus, as commercially produced frames were not available. The Spiegel-Wycis stereotactic frame was in fact built by Davis, an English machinist, in the workshop of the Temple University Medical Center in Philadelphia. There was also a whole array of Chinese-designed stereotactic equipment, the most prominent among these being

11

the XZ-I to XZ-V brain stereotactic apparatus by Jian-Pin Xu of the Anhui Provincial Hospital (1964–1977). This was not unlike the Guiot– Gillingham frame, small and simple in design, being anchored to the calvarium, and not requiring sophisticated supportive equipment [11,19,20]. However, only procedures within the small confines of one cerebral hemisphere were possible and a lower degree of precision was afforded. The FY85II, designed by the Xian Fourth Military Hospital in 1985, was quite similar in principle to the Todd-Wells and Leksell frames. The patient’s head was secured within the base ring. It was based on the arc principle and had a wider range of maneuverability, permitting bilateral hemispheric procedures with a higher degree of accuracy of within 2 mm. Other stereotactic equipment invented included the DZY-A from Nanjing and a frame by Wu SL from the Guangdong Minimally Invasive Neurosurgery Medical Center, Guangzhou, during the same period (> Figure 11‐8). In 1989, Da-Jie Jiang and Li Pan designed a stereotactic instrument incorporating computerized tomography(CT)andmagneticresonanceimaging(MRI) guidance (> Figure 11‐6 right). The HB-set

. Figure 11‐7 Dr Jian-Ping Xu with his stereotactic device in 1986 (left) and operating with his computer-assisted CT-guided equipment (right)

131

132

11

History of stereotactic surgery in china

. Figure 11‐8 Stereotactic device used by Jiang (left) and Wu SL in 1983 (right)

stereotactic equipment, the fruit of a collaboration between the Beijing Science and Engineering University and the Beijing Naval General Hospital, was launched in 1995 [21]. This later phase of intense activity in research and development of instruments was made possible by the modern economic and sociopolitical reform of the late Chinese leader Deng Xiao-Ping in 1978. Rapid acquisition of wealth, prosperity, and affluence in China after 1978 resulted in enhanced purchasing power, allowing practically unhindered access to Western technology. Accelerated growth in a very technology-dependent field such as neurosurgery inevitably ensued. Many hospitals have since acquired CTand high-resolution MRI instruments. Positron emission tomography (PET), single photon emission computerized tomography (SPECT) and magnetoencephalography (MEG) machines were also installed in some of the leading centers. Computer-assisted frame-based and frameless neuronavigational surgical procedures were performed. Some hospitals employed homemade systems. In the West, computer-assisted stereotactic neurosurgery was available as early as

1969. Digital CT- and MRI-image-guided stereotactic surgery was introduced in China in 1973 and 1980, respectively. Following Schaltenbrand-Wahren’s publication of the Atlas for Stereotaxy of Human Brain in 1977 [22] and Ronald Tasker’s release of the Physiological Atlas of the Thalamus and Midbrain Using Electrical Stimulation [23], Jia-Qing Yao et al. produced the Stereotactic Anatomy of Brain Gray Matter (in Chinese) for use by Chinese neurosurgeons in 1983. In 1992, the same author published the Applied Stereotactic Anatomy of the Human Brain with specific reference to the Chinese population [24,25].

Training Programs, Professional Organizations, and National Conferences The earliest generation of Chinese neurosurgeons received their stereotactic neurosurgery training abroad. Jiang-Ping Xu was trained in Moscow under the distinguished Russian

History of stereotactic surgery in china

pioneer stereotactic surgeon Dr Edvard I. Kandel from 1960 to1963. Cheng-Yuan Wu was a visiting scholar in stereotactic surgery for one year at the University of Utah, USA, with Dr M. Peter Heilbrun. Others like LZ Cheng, XM Fu, and ZP Ling were subsequently trained at Karolinska Hospital, Sweden, and Henri Mondor Hospital, Paris. Many of the leading stereotactic and functional neurosurgeons currently holding senior positions in major Chinese neurosurgical centers have received training in well-known international centers including UCLA, John Hopkins Hospital, Karolinska Hospital, and Hannover Hospital, among many others. After the first Chinese Stereotactic Neurosurgery Institute was established in Anhui Province in 1983 (> Figure 11‐9) by Jian-Ping Xu and Ye-Han Wang, indigenous stereotactic neurosurgery training program became available to native Chinese neurosurgeons with Dr Xu as the program director. A Computer-assisted Stereotactic Training Course was organized the next year. The Annual National Workshop on Stereotactic and Functional Neurosurgery was hosted by the

11

Anhui Provincial Stereotaxic Neurosurgical Institute in 1987. By 1986, the total number of Chinese-made stereotactic devices in use had reached 300, and total number of stereotactic surgeries exceeded 1,000. It is estimated that as many as 80% of the current practicing stereotactic and functional neurosurgeons have benefited from the Anhui workshops. At various intervals, other leading medical centers, e.g., Beijing Neurosurgical Institute, Beijing General Hospital of Armed Police Force, Tianjin General Hospital, Shanghai Huashan Hospital, and hospitals in Guangzhou and Harbin, offer training in stereotactic neurosurgical techniques. The Anhui Provincial Stereotaxic Neurosurgical Institute, in particular, has trained more than 400 neurosurgeons in stereotactic and functional neurosurgery to date. The Neurosurgery Specialty Society of the Chinese Medical Association (CMA) was established in March 1986 with Chung-Cheng Wang as the Chairman. Wang, born 1925, played a very pivotal role in modern neurosurgery in the PRC, having mentored more than one-third of the

. Figure 11‐9 The first Stereotactic Neurosurgery Institute in Anhui Province, China

133

134

11

History of stereotactic surgery in china

current generation of Chinese neurosurgeons. Apart from a very illustrious neurosurgical career, being the pioneer in brain stem microneurosurgery and the first to perform cerebral angiography in China during the impoverished postliberation and Korean War era of 1950s, he served in the Medical Corps in the Korean War against the US-led Allied Forces in 1952 and has been elected as representative to the People’s Congress of China (the Chinese equivalent of the Parliament). The Medal of Honor was bestowed upon him during the XII World Congress of Neurosurgery held in September 15–20, 2001 in Sydney, Australia. The Chinese Society of Stereotactic and Functional Neurosurgery was formed in July 1987 under the umbrella of the CMA. The first National Stereotactic and Functional Neurosurgery Conference in June 6–8, 1987 at Hefei, Anhui Province, was organized by the Neurosurgery Specialty Society of the CMA and attracted 155 participants with 85 papers presented (> Figure 11‐10). It has since been held seven times: May 16–20, 1990, in Chendu; May 9–13, 1993, in Dalian; May 12–16, 1997, in Beijing; August 1–4, 2001, in Harbin; June 6–10, 2004, in Yinchuan; June 26–30, 2006, in Huangshan.

In November 16–19, 2007, the First National Congress of Functional Neurosurgery was held in Xiamen. This was organized by the Stereotactic and Functional Neurosurgery Specialty Committee, Neurosurgery Association of the Chinese Medical Doctors Association (CMDA), a parallel organization to CMA. It was attended by more than 400 participants. The first National Congress for Brain Tissue and Neural Cell Transplantation was held in Kunming in January 1990. The Chinese Association of Epilepsy Surgery was established in 1990 and organized its first National Epilepsy Surgery Work-shop in the following year. In December 1998, the Guangdong Minimally Invasive Neurosurgery Medical Center organized the first National Minimally Invasive Neurosurgery Conference in Guangzhou. The biannual Shanghai International Symposium on Functional Neurosurgery is hosted by the Center for Functional Neurosurgery of the Shanghai Medical University. The Shanghai Medical University, founded in 1927 as the National Fourth Zhongshan University Medical College, was incorporated into the Shanghai Huashan Institute of Neurological Surgery (SHIN) in March 2000. Invited, distinguished international speakers to these national conferences and other meetings

. Figure 11‐10 The historic First National Stereotactic and Functional Neurosurgery Conference. Hefei City, Anhui Province

History of stereotactic surgery in china

have included Bjorn Meyerson, Bengt Linderoth (Sweden); Andres Lozano (Canada); Philip L. Gildenberg, Weiser, Philip Starr, Antonio.A.F.De Salles (USA); and J.P. Nguyen, Pr Pierre Cesaro (France). In recent years, Chinese neurosurgeons have increasingly made their presence felt in regional and international conferences such as the Congress of the Asian Society for Stereotactic, Functional and Computer-assisted Neurosurgery (ASSFCN), Congress of European Society for Stereotactic and Functional Neurosurgery (ESSFN), World Congress of the World Society for Stereotactic and Functional Neurosurgery (WSSFN), WFN World congress on Parkinson’s Disease and Related Disorders, Congress of Neurological Surgeons (CNS), and the American Association of Neurological Surgeons (AANS) meetings. Frequent scholastic exchange with overseas counterparts has further enhanced international collaboration.

Modern Chapter of Chinese Stereotactic and Functional Neurosurgery Within the half a century since stereotactic and functional neurosurgery began in China, remarkable progress has been made. However, there is relatively less emphasis on research, be it laboratory or clinical, no doubt due to the immense workload and the difficulty of gathering follow-up information from patients spread over such a vast countryside. Leading neurosurgery centers can now offer stereotactic and functional neurosurgical treatments with cutting edge technology comparable to the West, by neurosurgeons with impeccable credentials. The Beijing Tiantan Hospital with its Beijing Neurosurgical Institute is one of the world’s top three neurosurgical institutes and Asia’s largest center for neurosurgical treatment, training, and research. It was designated by the World Health

11

Organization (WHO) in 1982, together with the Shanghai Huashan Hospital, as the WHO Collaborating Centers for Research and Training in Neurosciences in China. The Shanghai Huashan Hospital was incorporated into the Shanghai Huashan Institute of Neurological Surgery (SHIN) with the Gamma Knife Hospital and two other affiliated hospitals in March 2000. The large number of practicing stereotactic and functional neurosurgeons became self-evident when close to 500 registered participants attended the First National Congress of Functional Neurosurgery in November 2007 in the southern city of Xiamen which overlooks the Taiwan Strait. Sophisticated modern neurosurgical treatments however remain largely the exclusive and privileged domain of the elite urban rich, as health insurance has yet to gain a foothold in this part of the world. Huge disparity still exists in wealth, education, and social welfare between the affluent cities of the eastern coastal provinces, and the relatively more deprived rural areas in the interior. The paradox exists that while urban China can boast of world-class hospitals and treatment, the rural poor do not have easy access to sometimes even basic medical facilities. It is commendable that the problem is being aggressively addressed by the Chinese central government through its emphasis on preferential developmental programs for the western regions. Providing adequate healthcare to one-fifth of the world’s population spread over such a vast country is a daunting task for any government indeed. Nevertheless, the huge population with seemingly unstoppable economic progress offers a golden opportunity and a rich substrate for a quantum leap of development of this technologydriven division of medical science. Acquisition of abundant clinical data permits derivation of useful observations and conclusions on treatment modalitiesfrom huge pools of patients. J.N. Zhang published 580 case reports on stereotactic intracranial procedures for Parkinson’s disease in 2000 [26], and S.B.Yuan reported on 1,431 cases

135

136

11

History of stereotactic surgery in china

of intracranial lesions treated with the Chinesedesigned rotating gamma system (OUR-XGD) in the Chinese Journal of Stereotactic and Functional Neurosurgery in 2001 [27], while 3,094 patients were treated with the Leksell Gamma Knife by Liang JC in Guangzhou up to 1999 [28]. The extreme degree of subspecialization within many of the large metropolitan or university units, the envy of many foreign neurosurgical centers, permits rapid development of subspecialty neurosurgery in China. Unencumbered by legislative regulatory constraint and working within a much less litigious environment compared to the West, Chinese neurosurgeons are quick to embrace new modalities of treatments, admittedly some still controversial, ahead of their European or American counterparts. The Beijing-based General Hospital of Armed Police Force, for example, established its Department of Neural Stem Cells Transplantation in March 2004 and has since treated close to 200 patients with strokes, traumatic brain injury, spinal cord injury, motor neuron disease, and cerebral palsy [29]. The Xishan Hospital in Beijing has an ongoing program on the implantation of olfactory ensheathing cells (OEC) from the olfactory bulb of aborted fetuses on patients with diagnoses ranging from amyotrophic lateral sclerosis and spinal cord injury to Parkinson’s disease. It has reportedly treated over 600 cases since 2001 [30,31], while in Europe, for example, the laboratory research by Geoffrey Raisman at the Institute of Neurology, Queen Square, London, on adult autotransplanted OEC on rats is currently still awaiting human clinical trials [32]. These nascent therapies have not yielded the same consistent and reproducible results of, for example, deep brain stimulation (DBS) in Parkinson’s disease. Psychiatric neurosurgery has largely fallen into disrepute under public and political scrutiny and clouded by controversy in the West for the past two decades. This was due partly to the risk of litigation, ironically sometimes from patients

rendered well enough by psychosurgery to initiate legal proceedings, and refusal of reimbursement by insurance companies. The 1986, the U.S. Office of Health Technology Assessment report which stated that ‘‘psychosurgery should be considered experimental as it has never been studied in a scientific manner’’ further discouraged its more widespread acceptance. However, we have witnessed its unabated development in China in the same period. For example, psychosurgery for the alleviation of drug dependence gained popularity in China from 2000 to 2004.

Frame-Based Surgery, Neuronavigation, and Robotics This has seen perhaps the most impressive growth since digital imaging, and the advent of stereotactic instrumentation has brought stereotactic surgery into the realms of many Chinese neurosurgeons, who like their Western counterpart have hitherto confined their works to general neurosurgery [33,34]. Whereas previously stereotactic imaging had to rely on angiography and ventriculography, identification of intracranial landmarks can now be made by noninvasive CT or MRI. Diagnostic tissue biopsies, evacuations of hematomas and abscesses, intracavitatory instillations of radioisotopes for tumors [35,36], e.g., combined 32P and Methotrexate chemotherapy for deep-seated gliomas, interstitial 192Ir brachytherapy for glioblastomas [37,38], and transplantations of neural tissues with minimally invasive techniques have been widely carried out in China. CT-guided neuroendoscopies have also been performed. In 1998, Tian ZM from the Beijing Navy General Hospital of People’s Liberation Army reported on 1,300 cases of CT-guided operations under local anesthesia using both the Leksell stereotactic frame and the indigenous HB-III instrument [39]. Intratumoral instillation of radionuclide and chemotherapeutic agent (BCNU) accounted

History of stereotactic surgery in china

for 780 and 24 cases, respectively. Lesioning of functional targets (101 cases), brain tissue biopsy (171 cases) and evacuation of intracerebral hematomas (155 cases) constituted the remainder. The Chinese-made NDY stereotactic frame has also been employed by some neurosurgeons. Frameless stereotaxy or neuronavigation permits neurosurgeons to perform stereotacticassisted volumetric excision of intracranial space occupying lesions accurately, greatly minimizing procedure-related risks [40–42]. It is now being used with intraoperative MRI at the Beijing Tiantan Hospital and Shanghai Huashan Hospital. Neuronavigation with functional MRI (fMRI) has been used in surgery near eloquent areas [43]. Neuronavigation-assisted neuroendoscopies have also been carried out with a high degree of success [44]. It is has become a standard inventory in neurosurgery operating suites in major neurosurgical units in Beijing, Shanghai, Guangzhou, Tianjin, Xian, and other cities. Neuronavigational systems available in China include the SurgiScope (Elekta), StealthStation (Medtronics), VectorVision (BrainLab), and the China-made ASA-610V and ASA-630V (Shenzhen Anke High Tech Co.) [45]. Imageguided, robot-assisted stereotactic system (CRAS HB1) developed by the Beijing Aeronautical and Astronautical Institute was used by Tian ZM of the Beijing Naval General Hospital in 1997 on 32 patients comprising 23 cases of intratumoral brachytherapy, 3 cases of tissue biopsy, and 2 cases each of evacuation of abscess and hematoma, achieving an instrument efficacy of 86% [46].

Surgery for Movement Disorders The first pallidotomy for Parkinson’s disease was done freehand in1959 by Zhong-Cheng Wang, who is the president of the Chinese Neurosurgical Society and the Beijing Neurological Institute. Wang designed the transorbital approach using trocar puncture of orbital roof, contralateral to

11

the side of tremor or rigidity, 4 cm from midsagittal plane aiming 10 superiorly and medially. An FG 20–22 needle was then advanced to the frontal horn, replacing 30–40 ml of cerebrospinal fluid (CSF) with filtered air. The same needle after being withdrawn, was then reinserted a few degrees vertically inclined from Reid’s base line (inferior orbital to superior external auditory meatus) and 10 deviated towards contralateral side to a depth of 9 cm. The pneumoventriculogram thus created confirmed placement of needle tip 2 cm posterior and 1 cm inferior to foramen of Munro, 2 cm lateral to mid-sagittal plane. After 0.5 ml of 1% Novocain confirmed favorable response, 0.5 ml of 40% Iodipamide was introduced. This simplified procedure was intended to bring pallidotomy into the hands of many doctors who may have to practice under relatively Spartan circumstances [10] (> Figure 11‐11). Two years later, Mao-Shan Wang’s stereotactic device was put to fruition and he carried out stereotactic alcohol ablation of globus pallidus, quite akin to the original chemopallidectomy that I.S. Cooper published in Science in 1955. (Cooper subsequently switched the target to the thalamus and reportedly performed over 3,000 cases of chemo-thalamectomies.) [47,48]. MS Wang published his stereotactic procedure ‘‘Surgical Treatment for Parkinsonian Syndrome’’ in the Chinese Journal of Surgery in 1961 [12]. Similar endeavors using self-designed stereotactic apparatus were undertaken by the pioneer surgeon Da-Jie Jiang, who published his twoyear preliminary reports on 20 cases of extrapyramidal system disease in the Chinese Journal of Neurology and Psychiatry in 1964. Jiang’s targets included globus pallidus, ventro-lateral nucleus, centro-median nucleus, nucleus reticularis, and internal capsule depending on the predominance of tremors, rigidity, and upper or lower limb involvement [14]. Localization was based on the Spiegel–Wycis atlas and coordinates [49]. Intraoperative confirmation of electrode placement was

137

138

11

History of stereotactic surgery in china

. Figure 11‐11 Dr Wang’s patient feeding with previously tremulous left hand. Handwriting in dots before (above) and after procedure of another patient, 1959 (with permission from CC Wang)

carried out in three stages: using 0.5 ml 1% Novocain instilled into target through electrode needle, electrical stimulation, and depth electrode recording. Parkinson’s disease constituted the largest category of conditions treated, and the early procedures were predominantly ablative in nature. A large series of papers was published by Guo-Dong Gao from the Xian Fourth Military University (1,478 cases) and by Zhang JN (580 cases) [26,50]. Following Backlund’s first clinical trials in 1982 and Madrazo’s 1987 report on open microsurgical adrenal medullary tissue transplantation to the striatum for parkinsonism demonstrating therapeutic benefit [51,52], Wa-Cheng Zhang et al. of the Beijing Xuanwu Hospital embarked on transplantation of adrenal medulla to the head of caudate nucleus for six patients with Parkinsonian tremors using a XZ-III stereotactic device in 1987, using postoperative CT scan to confirm placement of transplant tissue carriage in the head of caudate nucleus. CSF dopamine and normetanephrine levels were elevated to 1–2 times of presurgical assay, and clinical symptomatic improvements of tremors were documented [53]. In 1994, Wu CYet al. published their results of combined fetal substantia nigra

tissue transplantation and stereotactic thalamotomy in the British Journal of Neurosurgery [54]. Gamma knife thalamotomy (Vim, VO) using a 4-mm collimator delivering 130 Gy for the treatment of 58 cases Parkinson’s disease and other movement disorders was reported by Zhang Jie et al., claiming 80% good response over a follow-up period of up to nine years [55]. The first human microelectrode recording (MER) during functional brain surgery was reported by Albe-Fessard in 1961. MER was introduced in China in 1998 by Yong-Jie Li of the Beijing Institute of Functional Neurosurgery, Xuanwu Hospital. More than 2,000 cases of pallidotomies with CT or MR guidance have been carried out annually in China [50,56,57]. A significant proportion of those employed intraoperative MER for physiologic confirmation of electrode placement. Li published a review of 1,135 cases of surgical treatment of movement disorders in 2001 [58]. In 1972, Bechtereva N.P. of the former Soviet Union carried out therapeutic stimulation of the deep brain structures using intermittent external stimulation [59]. Siegfried and Benebid started DBS surgery for Parkinson’s disease in 1985 after the former unexpectedly noticed

History of stereotactic surgery in china

amelioration of Parkinsonian tremors from the implanted thalamic deep brain stimulator meant for chronic pain [60,61]. The U.S. FDA has approved DBS as a treatment for essential tremors, Parkinson’s disease, and dystonia in1997, 2002, and 2003, respectively. Led by Chung-Cheng Wang, the Beijing Tiantan Hospital performed the first DBS surgery for Parkinson’s disease in China in September 1998. Visits by Dr Philip A. Starr, University of California San Francisco (UCSF), and Dr Andres Lozano, Toronto Western Hospital, to China in 1999 helped DBS surgery, which gained further popularity. By 2003, more than 300 personal cases of DBS of subthalamic nucleus of Luys were performed by leading functional neurosurgeons like Jian-Guo Zhang, Yong-Jie Li (Beijing), and Bomin Sun (Shanghai). Other functional neurosurgeons like Kang-Yong Liu, Xiao-Wu Hu (Shanghai), Zhi-Pei Ling (Anhui), Shi-Zhong Zhang (Guangzhou), and Guo-Dong Gao (Xian) have also accumulated considerable

11

personal experience in DBS surgery. Their works have been variously published in Chinese Journal of Neurosurgery in 2002 [50,58,62,63]. There are more than 30 hospitals in China where DBS for Parkinson’s disease are regularly performed (> Figures 11‐12 and > 11‐13). The total number of cases done since 1998 has exceeded 1,000. In the Beijing Tiantan Hospital, Xuanwu Hospital, and Shanghai Ruijin Hospital, DBS treatment has also been extended to dystonia, Tourette syndrome, Hallervorden–Spatz disease, Meige’s syndrome, and chorea using subthalamic nucleus as target [26,64]. In 2002, Bo-min Sun used subthalamic nucleus of Luys for primary and tardive dystonia and achieved 90% 3 months to 3 years postoperative improvement based on Unified Parkinson Disease Rating Scale (UPDRS) and the Burke–Fahn–Marsden Scale [65]. Microelectrode recording were generally used in DBS surgery for intraoperative neurophysiologic targeting like in other overseas centers [66,67].

. Figure 11‐12 Deep brain stimulation surgery at the Shanghai Medical University (Fudan University) Huashan Hospital

139

140

11

History of stereotactic surgery in china

. Figure 11‐13 DBS electrodes in subthalamic nucleus. (Shanghai Huashan Hospital)

Stereotactic Radiosurgery Stereotactic radiosurgery was first introduced into China in 1993 when the Leksell gamma knife was installed in Wanjie Hospital in the northeastern port city of Qingtao. This was soon followed by the Beijing Tiantan and Shanghai Huashan Hospitals. There are more than 50 stereotactic radiosurgery centers in China. The Chinese-designed rotating gamma system OURXGD was launched in 1994 and relied on only 30 cobalt-60 sources instead of 201 in the Leksell system. The SGS-I stereospecific gamma ray whole body treatment system (> Figure 11‐14) has since been launched. It is estimated that more than 8,000 cases of stereotactic radiosurgery and radiotherapy are treated annually, with Beijing Tiantan Hospital alone accounting for more than 10,000 cases till December 2007. Currently, there are 17 Leksell gamma knife radiosurgery installations (compared to 35 in the USA), almost an equal number of LINAC X-Knife units, over 20 rotating gamma system (OUR-XGD) units, 1 Novalis (Brain Lab) ststem, and 4 CyberKnife (Accuray Inc.) systems in mainland China. The OUR-XGD rotating gamma

system and the SGS-I have been exported to countries such as Egypt, India, and Hungary. In 1999, Liang JC and Wu HX of the Guangzhou General Hospital of PLA reported on the gamma knife treatment of 3,094 cases of intracranial lesions including brain tumors (with or without cytoreductive surgery), arteriovenous malformations, and even functional targets [28,68]. From July 1995 to May 1998, they had treated 280 cases of arterio-venous malformations, of which 42 were Spetzler–Martin grade I, 68 grade II, 95 grade III, and 7 grade IV and grade V 4, with a high obliteration rate for grade I and II. Another large clinical series of 1,431 cases was published by Yuan SB of the Sichuan Gamma Knife Center, Chengdu Army Hospital, using the OUR-XGD rotating gamma system over a four-year period from January 1997 to January 2001 [27]. The results of the LINAC X-Knife treatment on 510 cases were documented by Wang LG in 2000 [69]. Gamma knife radiosurgery have been utilized for thalamotomy in Parkinson’s disease and other functional disorders [55]. It is worth noting that Lars Leksell actually conceived stereotactic radiosurgery in 1951 for the treatment of the functional disorder

History of stereotactic surgery in china

11

. Figure 11‐14 SGS-I: Chinese-made whole-body rotating gamma ray treatment system

of obsessive compulsive neurosis apart from tic douloreaux [9]. X-Knife radiosurgery for intractable epilepsy had been carried out by Qi ST on focal functional areas after preoperative electroencephalography (EEG), MRI, and PET evaluations [70].

Epilepsy Surgery Treatment of epilepsy in China can be traced to ancient times. Apart from Neijing (Yellow Emperor’s Inner Classic) 2000 years ago, there have been many medical classics dating back to Tang Dynasty (Qian Jin Yao Fang – The Invaluable Medical Script 652 A.D.), Sung Dynasty (Ji Sheng Fang Medical Script 1253 A.D.), Yuan Dynasty (Danxi Miscellaneous Comprehensive Medical Text 1481 A.D.) and Ming Dynasty (Treatment Yardstick 1600 A.D.), where traditional (TCM) treatments of epilepsy were described. Victor Horsley introduced surgery for medically intractable epilepsy in 1886. It is estimated that about one-quarter of epilepsy patients

become medically intractable, rendering them candidates for surgical intervention. Epilepsy surgery was accepted as an alternative treatment by the U.S. National Institute of Health Consensus Development Conference on Surgery for Epilepsy, March 19–21, 1990. In China, with a population of 1.3 billion, the total number of surgeries performed for medically refractory epilepsy had quadrupled from 600 before the year 2000 to 2500 in the year 2005 with a quarter from Beijing alone [71]. Review of the medical literature and hospital records indicate that the earliest documented works on epilepsy in China were in the 1950s, when Guo-Sheng Duan reported on lesionectomy for post-traumatic epilepsy with the aid of electrocorticography [72]. Krynauw RA first reported the removal of one cerebral hemisphere as the treatment for infantile hemiplegia [73]. Yu-Quan Shi of Shanghai First Medical College performed hemispherectomy under general anesthesia on four cases of severe infantile hemiplegia aged 3 years 5 months to 9 years in 1956. Pneumoencephalography demonstrated

141

142

11

History of stereotactic surgery in china

ipsilateral ventricular and cisternal enlargement, ventricular shift to contralateral side, as well as porencephaly. A normal contralateral ventricle was a prerequisite. EEG was used in cooperative patients. Hemispherectomy was done en bloc as opposed to Krynauw’s cruciate excision of the hemisphere in four blocks, sparing the caudate nucleus and thalamus (> Figure 11‐15). Shi observed improved seizure control, alleviation in aggressive behavior, and slight improvement in developmental IQ, but persistence of hemiplegia. Spasticity and hypertonia, though reduced, did not translate into improvement in dexterity of hand movements [74]. Ya-Du Zhao of Beijing Xuanwu Hospital also reported his experience on 12 cases of hemispherectomy and anterior temporal lobectomy from 1959 to 1963, employing intraoperative electrocortical recording and bipolar direct electrical cortical stimulation [75] (> Figure 11‐16). Shi and Zhao were considered the pioneers who laid the foundation of modern epilepsy surgery in China. (Ya-Du Zhao was the younger son of Yi-Cheng Zhao, the ‘‘founder of neurosurgery in China’’). Subsequent works were done by

Chen-Ji Liu of the Nanjing Military General Hospital and Zhi-Xun Wu of the Kunming Medical College in 1963. Jian-Ping Xu and Ye-Han Wang of the Anhui Provincial Hospital popularized stereotactic ablative epileptic surgery using homedesigned stereotactic equipment in the 1970s. In 1978, surgical treatment for epilepsy was finally made available in the western interior province of Sichuan by Li-Da Gao, Ge Wu, and ChangGui Zhou. After a quiescence of 10 years during the unfortunate Chinese Cultural Revolution (1966–1976), resurgence of epileptic surgery was made possible by the rapid socioeconomic development commencing 1978. Many procedures were undertaken, including temporal lobectomy, corpus callosotomy, neuroaugmentation (vagal nerve and cerebellar stimulation), and multiple vertical subpial transaction (MST) (Frank Morell, Rush-Presbyterian-St Luke’s Medical Center) [71,76–78]. Techniques in stereotactic corpus callosotomy and hippocampal resection were published by Jian-Ping Xu and Ye-Han Wang of the Anhui Provincial Stereotaxic Neurosurgical Institute in 1984 [79], while in 1994 Xiao AP et al. from

. Figure 11‐15 Pneumoencephalography showing left cerebral hemispheric atrophy, compensatory ipsilateral ventriculomegaly (left picture), and the medial surface of the excised left cerebral hemisphere (right picture). (DrYu-Quan Shi, 1956, Shanghai, with permission)

History of stereotactic surgery in china

11

. Figure 11‐16 Electrocorticography – unipolar lead tracing. Site A showed positive spike waves, electrical stimulation reproduced a subdued form of the original seizure. (Dr YD Zhao, Beijing, 1959, with permission)

the Nanjing Medical University reported 51 cases of stereotactic ablation of Forel H. Field (Mukawa J 1966) [80,81] and unilateral or bilateral amygdalotomy for 51 patients, aged 7–54 years, over a seven-year period since 1987 [82]. Bilateral cingulotomy and anterior capsulotomy were supplemented on 16 patients who had mental disorder. Procedures were done under local anesthesia except for four children. Intraoperative target localization was aided by pulsed electrical stimulation and acoustic impedance. Through similar works by C.C. Jiang and DJ Jiang of the Shanghai Huashan Hospital (1989) [83], Tang YL, and Zhang ZX, 82 cases (1990) [84] have been published. Gui-Sing Wang in 2004 used depth electrode for hippocampal EEG monitoring and stereotactic guidance in temporal lobe epilepsy surgery [85]. Neuronavigation and electrocorticography have been used in the resection of tumors causing secondary epilepsy [86,87]. Notable contributions were made by Qi-Fu Tan from the Hospital of Nanjing Military Area Command, who proposed guidelines on patient selection, preoperative assessment, operative results, and evaluation protocols, and also improved on the techniques of temporal lobectomy.

He performed corpus callosotomy in 1983 and Rasmussen’s functional hemispherectomy (Theodore Rasmussen, Montreal Neurological Institute) [88]. His results were published in Stereotactic and Functional Neurosurgery [89]. The spectrum of operated cases currently ranges from focal or partial epilepsy due to neoplasm to focal cortical dysplasia, hippocampal hemiatrophy, epileptogenic foci in temporal or frontal lobes, and multifocal epileptic zone located at or near eloquent cortex. Standard presurgical workup includes comprehensive neurosurgical, neurological, and neuropsychiatric assessment, electrophysiological studies including video EEG monitoring, digital imaging with MRI, and fMRI and MR spectroscopy where indicated [90,91]. Alterations in cerebral metabolism in the ictal and interictal period are documented with PET or SPECT [92]. MEG and implanted electrodes have also been employed [85,93]. Zhang G.J. of Beijing Xuan Wu Hospital [94] reported his experience on the application of long-term intracranial EEG monitoring using rectangular grids, linear strips, and stereotactically implanted flexible depth electrodes in epilepsy surgery in the Chinese Journal of Neurosurgery in

143

144

11

History of stereotactic surgery in china

2005 (> Figure 11‐17). Luan G.M. from the Beijing San-Bo Brain Science Institute pioneered low-power bipolar electrocoagulation on layer III of cerebral cortex for epileptogenic foci on or near eloquent cortex for patients in whom MST was otherwise indicated, and reported good results [95]. This has been increasingly adopted by other epilepsy surgeons. However, its longterm efficacy and delayed sequelae have yet to be fully elucidated. He and his colleague Yunlin Li carried out various combinations of procedures from lobectomy, hemispherectomy, corpus callosotomy, and vagus nerve stimulation to low-power bipolar electrocoagulation on the eloquent cortex on 77 patients with multiple epileptogenic foci. Intraoperative electrocorticography was employed. Fifty-three patients achieved class I and II seizure control, based on Dr Jerome Engel Jr’s classification on surgical outcomes [96]. Stereotactic radiosurgery in epilepsy surgery was reported by Qi-Fu Tan in 2001 [97]. S.T. Qi used the X-Knife (BrainLab) with EEG, MRI, and PET for intractable seizures from focal functional areas [70]. Treatment on 38 patients diagnosed with medial temporal lobe epilepsy

from January 1998 to December 2004 using the Chinese-made rotating gamma system (OURXGD) was reported by Yuan SB, with 73.68% overall efficacy (Engel I–III) [98]. The Beijing Tiantan Hospital took the lead by setting up the first independent epilepsy surgery unit in China, with a current annual surgical census exceeding 200. The number of hospitals with an epilepsy surgery unit in Beijing City alone has tripled from three in 1990 to nine in 2005. There are between 150 and 200 practicing epilepsy surgeons in China responsible for over 2,500 cases per year. Epilepsy surgery is now available in Nanjing, Guangzhou, Harbin, Chongqing, Chendu, Kunming Anhui, Wuhan, Shandong, Xinjiang, and Shijiazhuang, apart from Beijing and Shanghai. The National Epilepsy Surgery Society was formed in 1990, with the first National Epilepsy Surgery Workshop held in the next year in Qufu (birth place of Confucius). It has since been held four times on annual or biannual basis. The Chinese Newsletter of Epilepsy Surgery was published in 1992 with Qi-Fu Tan as the editor. The China Association Against Epilepsy (CAAE) was formed in June 2005. It has become a member

. Figure 11‐17 Electrocorticography in epilepsy surgery in twenty-first century China

History of stereotactic surgery in china

of the International League against Epilepsy (ILAE). Epilepsy surgery has featured prominently during six of the National Stereotactic and Functional Neurosurgery Conferences since 1987. Works by Chinese epilepsy surgeons are published in the Journal of Epilepsy Surgery, Journal of Asian Epilepsy in addition to the Chinese Journal of Stereotactic and Functional Neurosurgery. The second edition of the Textbook of Epilepsy Surgery edited by Qi-Fu Tan was released in 2006 [99].

Psychosurgery Although psychosurgery was performed in China by Tong-He Zhang of Xi’an in the 1940s, barely five years after the Portuguese Nobel Prize winner neurologist Egas Moniz conceived and performed the first operation for psychiatric disorder with neurosurgeon Almeida Lima on November 12, 1935 [100], this was followed by a lull of almost four decades. This was undoubtedly influenced by the events in neighboring fellow communist Soviet Union. Bekhterev and the father of Russian Neurosurgery Puusepp performed frontal leucotomy for maniac depressive psychosis and psychic equivalents of epileptics in 1906–1910, while classical leucotomies of Moniz and Lima for schizophrenia and severe pain were done from 1930s to late 1940s. Psychosurgery was banned in Soviet Union in1950 for ideological reasons [101]. Interests in psychiatric neurosurgery were rekindled in 1980s in a handful of Chinese hospitals in tandem with developments in the West [102]. Wu SL reported on 23 cases of schizophrenia treated with anterior cingulotomy in 1988 [103]. The first National Psychosurgery Conference was held in Nanjing in 1988, during which 542 cases of neurosurgical treatment for psychiatric disorders were presented. Procedures performed were anterior cingulotomy and amygdalectomies for various intractable mental illnesses including chronic schizophrenia and epileptosis. During the conference, the National

11

Clinical Guidelines for Psychosurgery were formulated, spelling out criteria for patient selection, informed consent, procedure types, and perioperative psychological assessments, among other issues. Since schizophrenia constituted the main bulk of operative cases, surgery expectedly did not result in amelioration of symptoms, just as Ballantine concluded in his retrospective report in 1989 on 198 patients who underwent anterior cingulotomy that schizophrenia and personality disorder responded least well to surgical treatment. A similar conclusion was made by Moniz [104,105]. Surgical option was not warmly received by psychiatrists who were never strong advocates of surgical intervention for their patients. The number of psychosurgeries dwindled progressively, and by the later half of 1990s many hospital had discontinued psychosurgery altogether. The revival of psychosurgery in China in the twenty-first century coincided with the widespread application of CT- and MRI-guided stereotactic surgery in the field of neurosurgery, allowing components of the limbic system, e.g., cingulate gyrus, amygdale, etc., to be accurately and safely approached [106]. Stereotactic limbic surgery, a more appropriate term than psychosurgery, was applied to the more responsive affective, anxiety, and obsessive compulsive disorders. A better understanding of the pathophysiological substrate of psychiatric diseases resulted in more widespread acceptance of psychosurgery. The French neurosurgeon Jean Talairach and colleagues first performed anterior capsulotomy for psychiatric disorders in 1949. Radiofrequency (RF) thermocoagulation stereotactic capsulotomy was subsequently developed by Lars Leksell. In 1999, Bomin Sun of Shanghai introduced MRIguided bilateral capsulotomy (> Figure 11‐18) for refractory obsessive-compulsive disorder, which he reported in the Chinese Journal of Neuropsychiatric Disorder in 2003. Capsulotomy-induced localized orbitofrontal subcortical metabolic changes in obsessive compulsive disorder were documented with PET (> Figure 11‐19) [107].

145

146

11

History of stereotactic surgery in china

. Figure 11‐18 Postoperative MRI. Capsulotomy in obsessive compulsive disorder. (Shanghai Huashan Hospital 1999)

A few cases of DBS for obsessive compulsive disorder have been carried out by Sun, targeting the anterior capsulum. Unilateral (right) lesion combined with DBS of the dominant (left) side appeared to yield better surgical outcomes. Clinical analyses of 138 cases of multitarget stereotactic thermocoagulation of amygdala, anterior cingulum, and anterior internal capsule for intractable psychosis have been reported by Xiao-Feng Wang and Ke-Ming Jiang in the Chinese Journal of Stereotactic and Functional Neurosurgery in 2003 [106]. Since 2000, psychosurgery for opiate addiction was carried out in some Chinese hospitals. For the few years till 2004, when it was finally banned for general clinical applications by the Chinese Ministry of Health because of public outcry from its socioethical controversy, more than 500 cases have been performed. From July 2000 to November 2004, 272 cases of stereotactic

ablation of nucleus accumbens for opiate addiction were performed at the Tangdu Hospital, Xian Fourth Military Medical University [108]. (Note: The Russians had chosen cingulate gyrus as the target.) Guo-dong Gao published the clinical study on the success and relapse in the initial 28 cases, claiming 65% good to excellent results over a mean follow-up period of 15 months [109]. Other workers have also targeted the medial septal diagonal band complex [110]. One case of successful bilateral DBS on nucleus accumbens was included in Xu Ji-Wen’s 27 case reports of neurosurgical treatment for drug addiction in 2005 [111].

Functional Neurosurgery for Pain Surgical treatment for pain had progressed from interruption of pain pathways to stimulation of

History of stereotactic surgery in china

11

. Figure 11‐19 From left: Preoperative and post-PET scan of a Chinese patient with obsessive compulsive disorder

pain-inhibiting pathways. Initial reports in the 1960s by Spiegel-Wycis, Ballantine, and, more recently, Wilkinson consisted of thalamotomy and anterior cingulotomy for chronic, intractable pain [8,112,113]. DBS of periaqueductal-periventricular gray and somatosensory thalamus for the relief of cancer pain and deafferentiation pain was reported by Richardson and Akil in 1977 [114]. Meta-analysis of 13 seriescomprising 1,114patients by Young RF et al. indicated a modest average long-term success rate of 60% [115]. It is currently performed in the United States as an ‘‘off label’’ (physician discretion) procedure. Neuroaugmentation for pain with the exception of Tsubokawa’s motor cortex stimulation (MCS) [116] is rarely performed in China [117]. Instead, the procedures were predominantly ablative in nature. Jiang-Ping Xu and Chung-Cheng Wang pioneered the percutaneous RF thermocoagulation for trigeminal neuralgia in China. A large series

of 1,860 cases was reported by Cheng-Yuan Wu et al. from the Qilu Hospital of Shandong University in 2004 [118]. A stereotactic basal frame for the 3D CT localization of foramen ovale and trigeminal stereoguide was designed. Excellent or good response was noted after selective percutaneous RF thermocoagulation in 96.3% cases, with a two-year recurrence of 24.8%. X-ray guidance, 3D CT, and neuronavigation enhanced the safety and accuracy of the procedure, overcoming the shortcomings of the freehand procedure. Microvascular decompressions for trigeminal neuralgia and hemifacial spasm are regularly carried out. Gamma knife radiosurgery for trigeminal neuralgia was reported by Mian-Shun Pan et al. of the Hefei Gamma Knife Hospital, Anhui Province, on 67 patients from 1997 to 2002, achieving 87.8% relief after an average three weeks [119]. Stereotactic thermocoagulation for central pain has been done since the early 1990s. Yang

147

148

11

History of stereotactic surgery in china

FM from Harbin reported on this procedure in 1992 [120].Ventriculogram and, in more recent cases, CT- or MR-guided RF lesion of centromedian nucleus and amygdala for chronic cancer pain on 46 patients have been reported by Jing GJ in 2002 [121,122]. Hu YS and Li YJ concluded in 2005 that a combination of bilateral anterior cingulotomy with mesencephalotomy resulted in more gratifying postoperative results based on the Visual Analog Scale and the McGill Pain Questionnaire assessment of patients [123]. Long-term response is still pending. Gamma knife stereotactic radiosurgery for the treatment of cancer pain has also been reported in a series of 322 patients by Jin Hu and Li-Jie Yi [124]. Frequent psychiatric overlay of chronic pain patients and the exceptional tolerance for pain unique to a race that has endured centuries of tremendous hardship can make objective verification of pain alleviation difficult in China.

Clinical and Laboratory Research Laboratory research on low-power bipolar coagulation of epileptogenic foci has resulted in its clinical application for intractable epilepsy from eloquent cortex [125]. This was first pioneered by Luan GM of the Beijing Brain Science Institute as an alternative to multiple subpial transaction in 2002 [95]. This has proven effective and is being adopted by many epilepsy surgeons especially in China. Neural transplantation research on the survival, migration, and differentiation, and the effects of Nerve Growth Factor (NGF) or Glial cell line derived neurotrophic factor (GDNF) on transplanted embryonal or bone marrow–derived stem cells and olfactory ensheathing cells in laboratory models of cerebral ischemia, spinal cord injury, and substantia nigra are being carried out [31,126,127], hopefully to be translated to clinical application. Effects of limbic leucotomy on quinpirole-induced obsessive compulsive behavior of rats drew parallel conclusions to human clinical results [128].

Further improvement on the robotic system for stereotactic neurosurgery previously launched in 1998 and 2002 is being carried out by the Robotic Institute of Beijing University of Aeronautics and Astronautics [46], while design and upgradation of software for targeting in stereotactic surgery continues [129]. The effect of controlled-release polymers of BCNU-PLA in experimental glioma in vivo and intratumoral radioimmunotherapy by radio-iodinated monoclonal antibodies form part of the cerebral tumor stereotactic brachytherapy research and experimental treatment by Li AB at the Beijing 304 Military Hospital [130].

Literature and Journals As the numerous clinical and scientific research papers published in the local journals each year are in the Chinese language mainly for local consumption, they are not accessible to foreigners outside China. However, with a better command of foreign languages, Chinese medical professionals have begun to publish in international journals over the past decade. The Chinese Journal of Stereotactic and Functional Neurosurgery was first published by the Anhui Provincial Stereotaxic Neurosurgery Institute in 1986, initially irregularly. It is now released bimonthly (> Figure 11‐5). The Chinese Journal of Minimally Invasive Neurosurgery is a monthly publication of the Guangzhou General Hospital of Guangzhou Military Region. The Journal of Chinese Neurosurgery, the official journal of the Chinese Neurosurgical Society, is published quarterly since 1985. Other related journals include the Journal of Epilepsy Surgery, Chinese Journal of Contemporary Neurology and Neurosurgery, Chinese Journal of Clinical Neurosurgery, Chinese Journal of Neurosurgical Disease Research, and Chinese Journal of Neuromedicine. Stereotactic and functional neurosurgery books and monographs (in Chinese) published include Stereotactic Anatomy of Brain Gray

History of stereotactic surgery in china

Matter by Yao JQ and Chen YM in 1980, Functional and Stereotactic Neurosurgery by Chen BH [131], Applied Stereotactic Anatomy of the Human Brain by Yao JQ and Dai HR in 1992, Brain Transplantation by WU CY in 1993, Stereotactic Radiosurgery by Chen BH [132], Textbook of Epilepsy Surgery edited by Tan QF in 1995 (2nd edition 2006), Minimally Invasive Neurosurgery by Ma LT in 1999, The Temporal Lobe Epilepsy Surgery by Lin Li in 2003, Modern Stereotactic Neurosurgery by Tian ZM in 1997, and the Chinese translation of Epilepsy Surgery edited by H.O. Luders and Y.G.Gomair (Lippincott, Williams and Wilkins, Baltimore, 2000).

Conclusion Napoleon Bonaparte of France (1804) once said: ‘‘Let China sleep. For when China wakes, it will shake the world.’’ In the last half century, we have witnessed the spectacular rise of China from obscurity to world prominence. As China integrates herself into the world community, Chinese medical professionals have redefined their roles in the international medical fraternity [133–144].

9. 10. 11. 12. 13.

14.

15.

16.

17. 18. 19. 20.

21.

References 1. Alt Kw, Jeunesse C, Buitrago-Tellez Ch, et al. Evidence for stone age cranial surgery. Nature 1997;387:360. 2. Han KX, Chen XC. The archaeological evidence of trephination in early China. Archaeology 1999;7:63-8. 3. Jia ZF. A brief history of the development of neurosurgery in China. Chin Med J (English) 1987;100:503-8. 4. Zhao YD, Zhao YL. Neurosurgery in the People’s Republic of China: a century’s review. Neurosurgery 2002;51:468-77. 5. Kwan (Guan) ST. Trigeminal neuralgia: diagnosis and treatment. Chin Med J (English) 1932;46:260-76. 6. Chang C. Neurofibroma of the gasserian ganglion. Chin Med J 1935;49:412. 7. Spiegel EA, Wycis HT, Marks M, Lee AS. Stereotaxic apparatus for operations on the human. Science 1947;106:349-50. 8. Spiegel EA, Wycis HT, Szekely EG, Gildenberg PL. Combined dorsomedial, intralaminar and basal thalamotomy

22. 23.

24.

25. 26.

27.

28.

11

for relief of so called intractable pain. J Int Coll Surg 1964;42:160-8. Leksell L. The stereotactic method and radiosurgery of the brain. Acta Chir Scand 1951;102:316. Wang CC, Huang KQ. A new operation for parkinsonian syndrome. Chin J Neurol Psychiatr 1960;6(2):80-1. Xu JP. Stereotactic application in neurosurgery. Acta Anhui Medical College 1963;6:228-31. Wang MS. Surgical treatment for parkinsonian syndrome. Chin J Surg 1961;9(7):524-5. Jiang DJ. Investigation of stereotactic brain surgery: design and application of a stereotactic instrument. Chin J Neurol Psychiatr 1964;8:238-43. Jiang DJ. Stereotactic operation for extrapyramidal system disease: a preliminary report of 20 cases. Chin J Neurol Psychiatr 1964;8:370-3. Riechert T, Mundinger E. Beschreibung und Anwendung eines Ziegerates fur sterotaktische Hirnoperationen. Acta Neurochirurg Suppl 1954;3:309. Talairach J, Hecaen H, David M. Lobotomie prefrontal limitee par electrocoagulation des fibres thalamo-frontales a leur emergence du bras anterieur de la capsule interne. In: Congress Neurologique International. Paris: Masson; 1949. p. 1412. Parera C, Cooper IS. A modification of chemopallidectomy guide. J Neurosurg 1960;17:547. Austin A, Lee A. A plastic ball-and-socket type of stereotaxic director. J Neurosurg 1958;15:264. Gillingham FJ. Advances in stereotactic and functional neurosurgery. New York: Springer; 1980. Xu JP. The beginning and development of stereotactic and functional neurosurgery in China in the last 25 years. Chin J Stereotac Funct Neurosurg 1990;3:3-5. Tian ZM. Modern stereotactic neurosurgery (Chinese). Beijing Chinese Science and Technology Press; 1997. Schaltenbrand G, Wahren W. Atlas for stereotaxy of the human brain. Stuttgart: Thieme; 1977. Tasker RR, Hawrylshyn P, Rowe IH, Organ LW. Computerized graphic display of results of subcortical stimulation during stereotactic surgery. Acta Neurochir (Wien) 1969;21:173-180. Yao JQ, Dai HR. Applied stereotactic anatomy of the human brain (Chinese). Shanghai Science and Technology Press; 1992. Yao JQ, Chen YM. Stereotactic anatomy of brain gray matter (Chinese). Beijing Science Press; 1983. Zhang JN, Wu SL, Zhang X, et al. Brain stereotactic procedures for Parkinson’s disease: 580 cases report. Mod Rehabil 2000;4:1212-13. Yuan SB, Lei J, Tang Y, Liao SC, Shun SQ, Deng ZP, Zhang XH, Pang XX. Preliminary reporting of rotating gamma system in 1431 cases of intracranial lesions. Chin J Stereotactic Funct Neurosurg 2001;14:209-12. Liang JC, WU HX, Jun ZH, Li L, Fu XP. Preliminary report of 3094 cases of intracranial diseases treated by

149

150

11 29. 30.

31.

32.

33. 34. 35.

36.

37.

38.

39.

40.

41.

42.

43.

44.

History of stereotactic surgery in china

gamma knife. Chin J Minimally Invasive Neurosurg 1999;4:9-12. General Hospital of Armed Police Force Beijing. http:// www.neuralstemcell.com.cn. Huang HY, Liu K. Neural regeneration and functional recovery of spinal cord injury after olfactory ensheathing cell transplantation. J Naval General Hospital (Beijing) 2001;4:65-7. Huang HY, Wang HM, Li BC, et al. Preliminary report of clinical trial for olfactory ensheathing cell transplantation in chronic spinal cord injury. Chin J Stereotac Funct Neurosurg 2004;6:348-50. Raisman J. Repair of spinal cord injury by auto transplantation of adult olfactory mucosal ensheating cells: translation from rat to clinical trials. Queen Square London: Spinal Repair Unit, Institute of Neurology; 2007. Hardy TL, Koch J. Computer assisted stereotactic surgery. Stereotac Funct Neurosurg 1982;45:396-8. Liu ZH. Latest development in stereotactic neurosurgical techniques. Chin J Neurosurg Dis Res 2003;2(1):1-3. Zha WG, Li AM, Fu XP. Stereotactic brachytherapy for cystic glioma in deep or eloquent brain areas. Chin J Minim Invasive Neurosurg 2006;11(10):474-7. Zhu FQ, LI AM, Xu F, Zhou YX, et al. CT guided stereotactic intracavitatory irradiation for intracranial cystic craniopharyngioma. Chin J Neurosurg 1998;14:142-4. Lin YC, Chen WJ, Zhu Ge QX. Combined CT- guided stereotactic interstitial radiotherapy of 32P and methotrexate chemotherapy for treatment of deep brain gliomas. Chin J Neurosurg 1996;12:216-8. Liu ZH, YU X, Guo Y, Cui YH, et al. The experimental and clinical preliminary studies of interstitial brachytherapy using iridium-192 on Glioblastomas. Chin J Neurosurg 1998;14:134-8. Tian ZM, Liu ZH, Li SY. Analysis of 1300 cases with CTguided stereotactic operations. Stereotac Funct Neurosurg 1998;70:147-8. Zhang X, Zhang J, Fei Z, et al. Neuronavigation-guided microsurgery for resection of brain tumors. Natl Med J China 2002;82(4):219-21. Zhao JZ, Cao Y, Lu Z, et al. Clinical evaluation of frameless stereotaxy in minimally invasive neurosurgery. Natl Med J China 2001;81:1042-5. Zhao YL, Wang CC, and Zhao JZ. Clinical use of navigation system in neurosurgical operations with 55 cases reports. Chin J Neurosurg 1998;14:274-6. Li GQ, Niu CS, Wang YH, et al. Functional MRI assisted neuronavigation guided surgery of intracranial tumors located in or near the motor cortex. Chin J Minim Invasive Neurosurg 2003;8(12):532-5. Jiang XF, Wang YH, et al. Neuronavigation assisted endoscopic procedures in neurosurgery. Chin J Stereotac Funct Neurosurg 2004;17(3):160-2.

45. Li GQ, Niu CS, et al. Application of ASA-610V neuronavigation system in minimally invasive neurosurgery. Chin J Contemp Neurol Neurosurg 2002;2(1):17-20. 46. Tian ZM, Wang TM, LI W, Chen MD. Location and mapping in robotic system for stereotactic neurosurgery. Chin J Biomed Engineering 2001;20(5):385-93. 47. Cooper IS. Chemopallidectomy. Science 1955;121:217. 48. Cooper IS, Bravo G, Riklan M, Davidson N, Gorek E. Chemopallidectomy and chemothalamectomy for parkinsonism. Geriatrics 1958;13:127-47. 49. Spiegel EA, Wycis HT: Stereoencephalotomy: thalamotomy and related procedures, vol. I–II. New York: Grune & Strattun; 1952-62. 50. Gao GD, Zhang H, Wang XQ, Liang QC. Indications of stereotactic and functional neurosurgery for Parkinson’s disease. Chin J Neurosurg 2002;18:12-4. 51. Backlund EO, Granberg PO, et al. Transplantation of adrenal medullary tissue to striatum in parkinsonism. First clinical trials. J Neurosurg 1985;62:169-73. 52. Madrazo I, Cuevas C, et al. Open microsurgical autograft of adrenal medulla to the right caudate nucleus in two patients with Parkinson’s disease. N Engl J Med 1987;316:831-4. 53. Zhang WC, Cao JK, et al. Neural transplantation with adrenal medullary tissue for tremors. Chin J Surg 1987;25 (11):650-2. 54. Wu CY, Zhou MD, Bao XF, et al. The combined method of transplantation of foetal substantia nigra and stereotactic thalamotomy for Parkinson’s disease. Br J Neurosurg 1994;8:709-16. 55. Jie Z, Ohye C, Shibazaki T. Gamma knife thalamotomy for the treatment of Parkinson’s disease and other movement disorders. Chin J Stereotac Funct Neurosurg 2005;18(6):354-7. 56. Wu SL, et al. Stereotactic neurosurgery for extrapyramidal disease. Chin J Nerv Ment Dis 1983;16(2):73. 57. Wu SL. Stereotactic surgery for tremors. Report of 507 cases. Chin J Stereotac Funct Neurosurg 1995;8(2):7-9. 58. Li YJ. Surgical treatment for movement disorders: a review of 1135 cases. Chin J Neurosurg 2001;6:350-3. 59. Bechtereva NP, Bondarchuk AN, Smirnov VM. Therapeutic electrostimulation of the deep brain structures. Vopr Neirokhir 1972;1:7-12. 60. Siegfried J, Lippitz B. Bilateral chronic electrostimulation of ventroposterolateral pallidum: a new therapeutic approach for alleviating all parkinsonian symptoms. Neurosurgery 1994;35:1126-9. 61. Benebid AL, Pollak P, Louveau A, Henry S, de Rougemont J. Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson’s disease. Appl Neurophysiol 1987;50:344-6. 62. Zhang JG, Wang CC, Zhang XY. Deep brain stimulation in idiopathic Parkinson’s disease. Chin J Neurosurg 2002;18(1):4-7.

History of stereotactic surgery in china

63. Sun BM, Liu KL, Lang LQ. Bilateral Deep brain stimulation of subthalamic nucleus in advanced Parkinson’s disease. Chin J Neurosurg 2002;18(1):8-11. 64. Zhang XH, Li YJ. Immediate and short term outcome after pallidotomy for intractable Tourette’s syndrome. Chin J Stereotactic Funct Neurosurg 2004;2:88-90. 65. Sun BM, Chen S, Zhan S. Subthalamic nucleus stimulation for primary dystonia and tardive dystonia. Acta Neurochir Suppl 2007;97(2):207-14. 66. Wang LX, Zhou XP, Hu XW, et al. MRI combining with micro electrode recording technology guided stereotactic surgery of Parkinson’s disease (270 cases). Chin J Stereotac Funct Neurosurg 2000;13(3):137-9. 67. Lee MK, Lee FC, Chee CP. The sunmed deep brain stimulation program for Parkinson’s disease: review after four years. XVII WFN World Congress on Parkinson’s disease and related disorders, Amsterdam. (Suppl); 2007. 68. Xu BT, Liang JC, Wang WM. Long term clinical efficacy of gamma knife radiosurgery for pituitary adenomas: a report of 487 cases. Chin J Minim Invasive Neurosurg 2006;11(6):244-6. 69. Wang LG, Guo Y, Zhang X. Linac X-knife stereotactic radio neurosurgery: 510 cases report. J Fourth Mil Med Univ 2000;21:1121-3. 70. Qi ST, Qiu BH, Yang KJ, Liu CY, Wang KW. Stereotactic radiosurgery treatment on focal area for intractable epilepsy. Chin J Stereotac Funct Neurosurg 2002;15:213-6. 71. Luan GM, Li YL. Epilepsy surgery in China: the history and current development. Neurology Asia 2007;12 Suppl 2:1-3. 72. Tan QF. Current status of epilepsy surgery in China. Chin J Stereotac Funct Neurosurg 2005;18(1):60-2. 73. Krynauw RA. Infantile hemiplegia treated by removing one cerebral hemisphere. J Neurol Neurosurg Psychiat 1950;13:243. 74. Shi YQ. Hemispherectomy for the treatment of infantile hemiplegia. Chin J Nerv Ment Dis 1959;1:48-51. 75. Zhao YD, Yang ZL, Tan YL. Surgical treatment of epilepsy. Chin J Neurol Psychiat 1965;9(4):325-9. 76. Kuang YQ, GU JW, et al. Combination of lesionectomy with multiple subpial transaction (MST) for intractable Epilepsy: 52 cases (Translation). Chin J Stereotac Funct Neurosurg 2004;02. 77. Morrell F, Whisler WW, Bleck TP. Multiple subpial transaction: a new approach to the surgical treatment of focal epilepsy. J Neurosurg 1989;70:231-9. 78. Yuan SB, Zhang J, Chen MZ, Zeng FJ, Chen LG. Multiple subpial transaction for intractable functional cortex epilepsy. Stereotac Funct Neurosurg 1998;70:92. 79. Xu JP, Wu HX. Amygdalotomy in temporal epilepsy: 10 case report. Chin J Nerv Ment Dis 1984;10:26-8. 80. Jinnai D, Mukawa J. Forel-H-tomy for the treatment of epilepsy. Confin Neurol 1970;32(2):307-15. 81. Mukawa J, Iwata Y, Kobayashi K. Forel-H field lesion effect on subcorticogenic and limbicogenic

82.

83.

84.

85.

86.

87.

88. 89.

90.

91.

92.

93.

94.

95.

96.

97. 98.

11

seizures- experimental studies. Neurologia Medicochirogica 1966;8:282-3. Xiao AP, Chang Y, Chen YY, et al. Stereotactic therapy for epilepsy. Chin J Stereotac Funct Neurosurg 1994;7: 21-22. Jiang CC, Jiang DJ, Yin SJ. Preliminary report of stereotactic callosotomy and/or amygdale nucleus for intractable epilepsy. Chin J Neurosurg 1989;5:260-2. Tang YL, Zhang ZX. The therapy of intractable epilepsy with stereotactic methods: a report of 82 cases. Chin J Neurosurg 1990;6:305-7. Wang GS, Xu JW, et al. The use of depth electrode in hippocampal EEG monitoring for localizing the epileptogenic zone in temporal lobe surgery. Chin J Stereotac Funct Neurosurg 2004;17(5):271-3. Shi YW, Mu J, Shi JJ, Gu F. Role of intraoperative electrocorticography in epilepsy surgery (Translation). Chin J Stereotac Funct Neurosurg 2007;20(3):165-6. Li TD, Bai HM, Jiang XX. Resection of brain tumors with epilepsy by electrocorticogram. Chin J Stereotac Funct Neurosurg 2004;17(2):85-7. Villemure JG, Rasmussen T. Functional hemispherectomy: methodology. J Epilepsy 1990;3 Suppl:177-82. Tan QF, et al. Long term results of functional hemispherectomy for intractable seizure. Chin J Stereotac Funct Neurosurg 2000;75:90-5. Jin LR, Wu LW, Gao W, et al. Ictal video-EEG monitoring in presurgical evaluation for intractable temporal epilepsy in 15 cases. Chin J Neurol 2002;35(3):132-4. Liang SL, LI AM, et al. Usefulness of 128 channels preoperative prolonged video-EEG in locating epileptogenic zone. Chin J Stereotac Funct Neurosurg 2003;16 (4):206-9. Wang HM, Zhang GP, LI L, et al. Clinical application of interictal SPECT in epilepsy surgery. Chin J Stereotac Funct Neurosurg 2004;17(5):268-70. Zhu D, Li L, Hua G, Guo J. Neuronavigation with magnetoencephalography for epilepsy surgery. Chin J Stereotac Funct Neurosurg 2005;18(3):155-7. Zhang GJ, LI YJ, et al. Application of long term intracranial EEG monitoring in epilepsy surgery. Chin J Neurosurg 2005;8:8-11. Li YL, Luan GM. A new method to treat functional intractable epilepsy: Introduction of bipolar electrocoagulation technique. Chin J Stereotac Funct Neurosurg 2002;3:265-8. Engel J, Jr, Van Ness PC, Rasmussen TB, Ojemann LM. Outcome with respect to epileptic seizures. In: Engel J, Jr, Surgical treatment of the epilepsies. New York: Raven Press; 1993. p. 609-621. Tan QF. The stereotactic radiosurgery in epilepsy. Modern Rehabilitation 2001;1:105. Yuan SB, Wu W, Liang X, et al. The rotating gamma knife for medial temporal lobe epilepsy (report of 38 cases). Chin J Stereotactic Funct Neurosurg 2007;20(1):10-14.

151

152

11

History of stereotactic surgery in china

99. Tan QF. Epilepsy surgery (Chinese). Nanjing University Press; 1995. 100. Moniz E. Prefrontal leucotomy in the treatment of mental disorders. Am J Psychiatry 1937;93:1379-85. 101. Lichterman BL. History of psychosurgery in Russia. Acta Neurochirugica 1993;125:1-4. 102. Binder DK, Iskandar BJ. Modern neurosurgery for psychiatric disorders. Neurosurgery 2000;47:9-23. 103. Wu SL. Bilateral stereotactic anterior cingulotomy for schizophrenia: a report of 23 cases. Chin J Neurosurg 1988;4:83-6. 104. Ballantine HT, Jr. Historical overview of psychosurgery and its problems. Acta Neurochir Suppl (Wien) 1988;44:125-12. 105. Feldman RP, Goodrich JT. Psychosurgery: a history overview [legacies]. Neurosurgery 2001;48(3):647-59. 106. Wang XF, et al. The clinical analysis of intractable psychosis treated with stereotactic techniques: report of 138 cases. Chin J Stereotac Funct Neurosurg 2003;16(4): 199-202. 107. Sun BM, Guan Y, Lang L, et al. Capsulotomy induces localized orbitofrontal and subcortical metabolic changes in obsessive compulsive disorder (abstract). Am Assoc Neurol Surg 2001;4 Toronto. 108. Wang XL, He SM, Li J, et al. Comparative study of reasons and influential factors on relapse after abstinence. Chin J Min Invas Neurosurg 2006;8:11. 109. Gao GD, Wang XL, He SM, et al. Clinical study for alleviating opiate drug dependence by a method of ablating the nucleus accumbens with stereotactic surgery. Stereotac Funct Neurosurg 2003;81:96-104. 110. Wang KW, Qi ST, Yang KJ. Medial septal diagonal band complex: A new target point of stereotaxic surgery for psychic dependence to opiods (report of 34 cases). Chin J Minim Invasive Neurosurg 2006;11(3):112-5. 111. Xu JW, Wang GS, Zhou HY. Neurosurgical treatment on alleviating heroin psychological dependence. Chin J Neurosurg 2005;21(10):19-22. 112. Ballantine HT, Jr, Cassidy WL, Flanagan NB, et al. Stereotaxic anterior cingulotomy for neuropsychiatric illness and intractable pain. J Neurosurg 1967; 26:488-95. 113. Wilkinson HA, Davidson KM, Davidson RI. Bilateral anterior cingulotomy for chronic non cancer pain. Neurosurgery 1999;45:1129-36. 114. Richardson DE, Akil H. Pain reduction by electrical brain stimulation in man.1. Acute administration in periaqueductal and periventricular sites. J Neurosurg 1977;47:178-83. 115. Young RF, Rinaldi PC. Brain stimulation in pain. In Levy RM, North RB, editors. The neurosurgery of chronic pain. New York: Springer 2003. 116. Tsubokawa T, Katayama Y, Yamamoto T, Hirayama T, Koyama S. Chronic motor cortex stimulation for the

117.

118.

119.

120.

121.

122.

123. 124.

125.

126.

127.

128.

129.

130.

131. 132.

treatment of central pain. Acta Neurochir Suppl (Wien) 1991;52:137-9. Zhao CS, Luo H, Sun BM. Chronic electrical motor cortex stimulation for intractable central pain. Chin J Stereotac Funct Neurosurg 2004;17(4):345-7. Wu CY, Meng FG, Wang HW, et al. Selective percutaneous radiofrequency thermocoagulation for treatment of trigeminal neuralgia: 1860 cases report. Chin J Neurosurg 2004;20:55-8. Pan MS, Ling ZP, Wang P, Zhen HM. The clinical study on gamma knife radio surgery for trigeminal neuralgia. Chin J Stereotac Funct Neurosurg 2004;17 (6):358-61. Yang FM, Yang SC, Lian YZ, Shu J, Zhao B. Treatment of central pain with stereotactic radiofrequency thermocoagulation. Acta Harbin Med Univ 1992;26:188-9. Jing GJ, Yang KY, et al. CT-guided brain stereotactic therapy of chronic cancer pain: report of 35 cases. Mod Rehab 2001;5:97-98. Jing GJ, Yang KY. Brain stereotaxic therapy for chronic cancer pain by thalamotomy (Chinese). J Sun Yat Sen Univ (Med Sci) 2002;23(2):13-7. Hu YS, LI YJ. Stereotactic neurosurgery for cancer pain. Chin J Pain Medicine 2005;11(4):197-200. Hu J, Yi LJ. The treatment of cancer pain with stereotactic radiotherapy. Chin J Pain Medicine 2002;8 (4): 195-7. Yang ZH, Luan GM, Zhang Y. The modal building and research of temporal lobe epilepsy. Chin J Neurosurg 2005;8:8-11. Wang Y, Duan DY, Xu QY. Survival, migration and differentiation of neural stem cells after transplantation into the brain. Chin J Biotechnology 2004;11: 13-17. Yu LH, Kang DZ, Lin JH. Orient migration of intravenous administration of bone marrow stromal cells after spinal cord injury in adult rats. Chin J Stereotac Funct Neurosueg 2006;19(1):17-20. Guo CL, Zhao AJ, Song J, Liu SJ. The effect of stereotactic limbic leucotomy lesion on obsessive compulsive disorder in rats. Chin J Stereotac Funct Neurosurg 2006;19(1):9-12. Hu ZY, Zhao XZ, et al. Design and application of soft ware for targeting thalamus and basal ganglia in stereotactic surgery (Chinese). Acta Academiae Medicinae Militaris Tertiae 2003;25(11):1019-20. Xu XN, Wang JH, Lu G, et al. Controlled release polymers of BCNU-PLA against experimental glioma in vivo. Chin J Stereotac Funct Neurosurg 2004;17(5): 280-3. Chen BH. Functional and stereotactic neurosurgery (Chinese). Inner Mongolia People’s Press; 1988. Chen BH. Stereotactic Radiosurgery (Chinese). Beijing Press; 1994.

History of stereotactic surgery in china

133. Anderson WS, Lenz FA. Surgery insight: DBS for movement’s disorders. Nature Clinical/Practice Neurol 2006;2:310-20. 134. Chou SN. Perspectives in international neurosurgery: a glimpse of neurosurgery in China. Neurosurgery 1978;3:120-2. 135. Gildenberg PL. Stereotactic surgery- the past and the future. Stereotac Funct Neurosurg 1998;70: 57-70. 136. Li P, Wu BJ, Nan Z, et al. Treatment of functional disorders with gamma knife radiosurgery. Stereotac Funct Neurosurg 1998;70:102-3. 137. Ma LT. Minimally Invasive Neurosurgery (Chinese). Wuhan: Huazhong Science Publisher; 1999. 138. Tan QF, Sun KH, Sun KJ. Results of surgical treatment in 76 patients with temporal lobe epilepsy. Stereotac Funct Neurosurg 1998;70:91.

11

139. Wang YH, Dong YJ, and XU JP. Stereotactic neurosurgery: past and present. Chin J Stereotac Funct Neurosurg 1986;1(1):46-52. 140. Wu CY, Wang YH, Meng FG, Liu YG. Development of stereotactic neurosurgery in China. Neurosurgery 2005;56:851-60. 141. Yi SY, Wu CY. Brain tissue transplantation (Chinese). People’s Hygiene Press; Beijing: 142. Zhang K, Zhang JG, Ma Y, et al. Subthalamic deep brain stimulation in the treatment of secondary dystonia. Chin Med J 2006;119(1):2069-74. 143. Zhang YQ, Li YJ, et al. Surgical treatment for adult onset dystonia: analysis of 16 cases. Chin J Min Invas Neurosurg 2006;11(2):121-5. 144. Tian ZM, Lu WS, Wang TM, et al. Application of a robotic telemanipulation system in stereotactic surgery. Stereotact Funct Neurosurg 2008;86:54-61.

153

9 History of Stereotactic Surgery in France A. L. Benabid . S. Chabardes . E. Seigneuret

Introduction The history of stereotaxy is part of a larger perspective of a methodological approach that is therapeutic and focuses on the search for precision. The search for precision implies the recognition and marking of targets (taxonomic version of the etymology of the word Stereotaxy, from taxis: order) as well as to the tactic act, which is the achievement, at least in human stereotaxy, of this approach (tactic version of the etymology of the word stereotaxy). The common denominator of these two definitions is the space (from the Greek Stereos: solid, volume), which by itself would define the methodology, based on the spatial coordinates of a point that will be called the target. This etymological duality corresponds in fact to a historical perspewctive, as for the first time, in 1917, the need to precisely recognize and localize the various spatial structures of the brain led Horsley and Clark [1] to design an instrumental method aimed at quantifying cerebral space, in order to attribute precise coordinates to the different structures that the anatomo physiologists were studying at that time. This taxonomy approach led to the development of an instrument and a method, and then to the elaboration of the concept of the surgical act based on exact location. This corresponded in fact to the tactic version of the etymological definition of stereotaxy, even if it has been, historically, only secondary. Having designed an apparatus and developed a method, one tended to build on these two concrete elements a philosophy, or at least a state of mind. This constitutes the most interesting, maybe the #

Springer-Verlag Berlin/Heidelberg 2009

most noble, part of the history of stereotaxy. This history has been the reflection of the complex interaction, depending upon circumstances, between the technical means of the moment and the therapeutic needs, as well as on pharmacological alternatives. This process is not specific to stereotaxy. It characterizes every approach of Homo Faber, which tries to solve his current problems, on the bases of the know-how which is available. He often stumbles on technological bottlenecks, which impede the development of methods, and even make it transitorily disappear, until the advance of knowledge in other domains provides the key, which will open the lock. A new momentum of development is therefore observed until the time when a new obstacle stops the process again, or when the need disappears, often because advancements of knowledge in other domains have brought more satisfactory solutions. Stereotaxy is at the crossroads of industrial technology, of surgical technology and therapeutic needs, themselves strongly enclosed in the domain of neurosciences, which, as we know, is undergoing rapid evolution. It is therefore not surprising to see that its history has been chaotic, and it can be foreseen that it will become even more complicated.

Innovation Comes from Necessity: History of the Development of the Stereotactic Frame In technological evolution, as in any kind of method, development is possible only if the need exists. The evolution of the need depends

98

9

History of stereotactic surgery in france

on the evolution of sciences and related disciplines. The need to discover the origin of an idea and identify its conceptual father depends on the value of this idea. There is a rich literature devoted to determining the paternity of stereotactic apparatuses, quite often in a chauvinist perspective. This need witnesses the importance of stereotaxy in the world of neurosciences, as it is easy to recognize its impact on our thinking and practice, in experimental neurophysiology as well as in clinics. This chapter could be included in this international competition, thanks to Professor Grellier in Nice who retrieved a document and was kind enough to give it to us. It proves that the stereotactic frame, and therefore the stereotactic method and practice, was invented in France at the end of the nineteenth century. In a paper published on 27 November 1897, in the review L’ Illustration [2], there is a very detailed description of it, in a scientific style which is not often used in public magazines (but it is probable that the culture of the public at that time was more scholarly than nowadays). The procedure was performed in a laboratory of the faculty of medicine in Paris, where the inventor had set up a system that could be anchored by pins to the skull of the patient presenting with projectiles (bullets or shrapnel pieces). This system featured a topological radiology modality oriented in space, consisting of two Crooke’s tubes and two photographic film supports mounted orthogonally. The radiographic antero-posterior and lateral projections of the head of the patients that were obtained made it possible to localize, as on an analytical geometry diagram, the presence of opaque foreign bodies, generally projectiles, even if they were not in teleradiological conditions. The figure, > Figure 9‐1 presented in this article of L’ Illustration is of remarkable precision and establishes without any doubt the feasibility of this approach, and of its precision, under the appearance of a frame, which could be very well compared to the frame of Horsley and Clark, or even to the Leksell frame, which is wellknown nowadays. The article reports that two interventions were successfully

performed, and reported in the Academy of Medicine by Marey (the physiologist). One cannot say whether this invention inaugurated either stereotaxy or interventional neuroradiology, but it is witnesses that the need to navigate within the brain was manifested a long time ago, whenever it was necessary to perform an intervention inside it. It seems that the encephalometer of Zernov (1889) [3], used in surgery by Altukhov 2 years later (1891) [4], aimed at the same goal of reaching intracranial structures, but without introducing in the approach a precise methodology of localization. It is more classical to quote at the origin of stereotaxy the publication in 1908 of Horsley, neurophysiologist and neurosurgeon, and Clark, mathematician, probably because their publication has given, in a scientific review known and read by their peers, the description of the apparatus, a stereotactic atlas of the monkey brain, and the method of electrolytic lesion by constant current. Ten years later, Mussen, the engineer who had worked on this frame, manufactured a version that he had designed, and then stored in his attic, wrapped in a journal, the headline of which helped to date this invention [5,6]. It was only in 1947 that Spiegel and Wycis [7] reported the use of an apparatus that allowed intraoperative X-rays, and coined the term stereoencephalotomy. This new approach allowed for the first time the mortality after operations to drop to about 2%. Ever since, the evolution of the stereotactic frames has not stopped, following trends and fashions, which accelerated its developments, and its adaptations to new indications. Two main categories of frames were developed, each favoring a modality of approach to the target. The Goniometric frames, putting the target at the pre-established center of an arch, are headed by the Leksell frame, followed by those of Richiert and Mundinger, and Todd and Wells, which finally produced the frames of Brent Robert Wells (BRW), and Cosman Robert Wells (CRW). The Cartesian frames on the contrary have developed orthogonal approaches from the lateral and the anteroposterior sides of the head, such as

History of stereotactic surgery in france

9

. Figure 9‐1 Upper right drawing: corresponds to the upper left photograph. The system, is made of:A frame fixed on the head by a cast. Three rods are firmly pressed on the forehead and on the cheek bones–Two photographic films will be successively placed on one side–On the other side two Crookes tubes (X-ray) which can be oriented–X-ray pictures are taken with one of the Crookes tubes. This is repeated with the other tube and another film–The system is removed from the head, the extremities of the three rods are tattooed on the skin, and the spatial position of the bullet is obtained at the intersection of two threads used to join the focus of the tubes to the images on the films, with respect to the three skin fiducials. Lower right drawing: corresponds to the lower left photographThe extremities A, B, C and D of four sliding rods which are adjusted such as to touch the skin fiducials (or face markers) for A, B, and C, and to the target/bullet for D. The length of the D rod represents the depth of the target/bullet and will guide the surgeon during the intracerebral procedure–This “Operating Compass” can be transported to the operating theatre, in the hospital or at the patient’s house. When it is applied on the face markers, the rod D points the direction and shows the distance to the target

99

100

9

History of stereotactic surgery in france

the Talairach frame, as well as those of OlivierBertrand, and of Hitchcock. Designs to adapt the goniometric approaches to the Talairach system have been made for individual users [8].

Introduction in France of the State of the Art of the Stereotactic Method After the reports of Remy and Contremoulins in 1897, the next mention of stereotaxy in France is found in the early 1950s about movement disorders (treated by ansotomy, pallidotomy and thalamotomy), [9–13], psychosurgery by lobotomy [14–16] and pain [17–24], using the conventional frames, methods and targets available in the western world. The French neurosurgeons practiced functional neurosurgery as a part of their general activity, showing special interest in these methods.. Some were especially attracted by the field and developed their own methods, such as ansotomy and campotomy for movement disorders [25–26], their frames [27–29] and their anatomical charts and atlases [30–34]. Among them would emerge, in academic institutions and practices, some who would provide such important contributions that they would make a profound mark on French stereotaxy.

Visionary Inputs of Two Giants Against this background of random practice and approaches, two main schools emerged and set the rules which have not only changed French stereotaxy but have had a real worldwide impact. They were inspired and led by two giants: Gerard Guiot at Hospital Foch, in the Parisian suburb of Suresnes, and Jean Talairach at Hospital SanteAnne, in Paris, who have educated and trained most of the French functional neurosurgeons and influenced many of the foreign masters in this field.

The Recognition of the Benefits of Multidisciplinarity: G. Guiot and D. Albe-Fessard Besides his tremendous input in neurosurgery at many levels, including pioneering work in pituitary surgery, Gerard Guiot (1912–1988) extended to all aspects of his practice an obsessional search for elements to improve his practice and results. In his functional neurosurgical practice, from pain to movement disorders, he needed to use every means to improve the precision of localization. He introduced the electrophysiological method into stereotactic procedures with the help of neurophysiologists such as Denise AlbeFessard and G Arfel. The use of intraoperative micro-electrophysiological recording has incomparable value, and was strongly stressed by the French stereotactic school in the third quarter of the twentieth century [11–13,27,35–38]. Its use was validated when it was clear that there was a correlation between efficacy, lack of complications, and the precision of the placement of the lesion, which was then used as the therapeutic tool. However, the importance of intraoperative neurophysiology has further decreased, for several reasons. The interest in stereotaxy has decreased because of the advent of levodopa, the expertise required an equipment not being available for neurosurgeons. Electrophysiology also appeared to be obsolete, or useless, because the target became more visible with the new imaging methods. This wrongly suggested that it was sufficient to aim at the structure to reach its function. This is true for the Pallidum and for the Subthalamic Nucleus, but it is not the case for the subdivisions of the Thalamus and for new targets such as the Pedunculopontine Nucleus (PPN), which are not visible and where the functional site has to be discovered through electrophysiology. Despite the advances in modern imaging, there are distortions in MR images, and displacements of cerebral structures during surgery, particularly during the progression of the

History of stereotactic surgery in france

electrodes. The functional target which is related to the efficacy of chronic stimulation cannot be reached without additional investigations. The recent development and the new interest in functional neurosurgery, particularly for movement disorders, the need for precision and safety, and the possibility to mimic the therapeutic effects of chronic stimulation during surgery, have given back intraoperative electrophysiology its double role. As an exploratory method, it provides the characteristic signature of the neuronal set through the morphology of the action potentials, their discharge pattern, and the activity evoked by external stimuli (proprioceptive, auditory, visual). As a therapeutic method, it reproduces accurately the effects which would be observed over a long term and allows the functional recognition of the target. It has become part of the classical panel of methodology in neurosciences. The discovery during those explorations of the differential effects of stimulation at high and low frequency has led to the development of methods of chronic deep brain stimulation at high frequency [39–47]. This development would not have been possible, or at least been long delayed, if implantable stimulators did not already exist, having been developed for the treatment of pain [23,48,49]. There was a long and disappointing inefficacy during which it had slowed down. The development of new applications to the treatment of movement disorders has re-motivated the industry to redevelop flexible electrodes and programmable stimulators.

The Reconsideration of an Unsatisfactory Situation: Jean Talairach Jean Talairach (1911–2007) could be described as a psychiatrist believing in psychosurgery and feeling that surgery was too serious to be left to neurosurgeons. He redesigned a stereotactic frame and raised it to the level of a method, if not a philosophy;

9

he built his own stereotactic atlas. When psychosurgery went out of favor, he had the spirit to refocus his stereotactic doctrine, his skills and his tools, to new applications, thereby opening new avenues such as a totally new vision of the surgical treatment of epilepsy. When movement disorders also went out of the field of stereotaxy, after levodopa was introduced as a treatment, he shifted gears and used his methodology to create a new field.

Stereotactic Biopsies The fate of a method depends on the need for it. When an outside phenomenon, such as a pharmacological newcomer, occurs, which brings, at least for a given period, a satisfactory solution, the need for the method disappears and sends it to oblivion. At the same time, the understanding that some pathologies, such as brain tumors, are not adequately taken care of by classical surgery and could eventually respond correctly to general treatments, such as chemotherapy or radiotherapy, induces the application of this forgotten, or nearlyabandoned, method to a totally new field: this is what Jean Talairach and his associates did when they introduced stereotactic biopsy, at a time where movement disorders needed less surgery as levodopa had come and provided a very attractive treatment. The school led by Jean Talairach at Sainte Anne must take credit for the development of stereotactic biopsies, for multiple reasons [50–54]. The growing awareness in the middle of the twentieth century that brain tumor resection was not always efficient or useful and that it was sometimes sufficient and less invasive to treat brain tumors by radiotherapy or chemotherapy had stressed the necessity to obtain the pathological diagnosis before applying those nonsurgical treatments. In addition to providing the right diagnosis, and sometimes to errors being corrected, multiple staged stereotactic biopsies allowed determining the extent of the lesion, particularly at the time when

101

102

9

History of stereotactic surgery in france

computerized tomography did not exist. Currently, using modern imaging, this need for the determination of the extent has diminished, allowing a decrease in the number of samples to the minimal necessity to obtain the histological signature, for instance, taking advantage of the recent demonstration that oligodendroglioma are chemosensitive when they bear the genetic mutation in 1p19q.

Brachytherapy [55–61] The use of ionizing radiations, in all their forms, has always played an important role in the therapeutic function of stereotaxy. The Parisian school of Jean Talairach had very early taken advantage of the radionecrotic properties of isotopes to create lesions with a reasonably foreseeable size: using Yttrium 90Y, mainly beta emitter, it was possible, because of its reduced propagation, to create a lesion of about 5 mm in diameter, in the place where the seed had been deposited under radiological control. This was used to replace electrolytic lesions for functional neurosurgery. This had also allowed Jean Talairach to develop methods of pituitary freination by Gold 198Au in the treatment of diabetic retinopathy by pituitary stereotaxy, based on the empirical observation, following the occurrence of a Sheehan syndrome, of the amelioration of this severe complication of diabetes. These indications of major hormonal surgery were also responsible for the concept, design and realization of the pituitary stereotactic frame. These methods, which led to very satisfactory results, later disappeared, following the advent of various forms of hormonal suppressive chemotherapy, similarly efficient and easier to manipulate. In the 1970s appeared the need to have a more focal treatment of brain tumors. Jean Talairach, along with Gabor Szikla, using Iridium 192Ir, introduced stereotactic Curitherapy, (named in

France from the multiple Nobel Price winner Marie Curie), in parallel with the German school, particularly in Freibourg with Riechert and Mundinger. In the literature in English, particulary in the United States, the term brachytherapy has been coined to better express the short distance effects of this therapeutic approach. This whole field of interstitial irradiation was undertaken along with experimental approaches and careful postoperative control and follow-up, as well as extensive histological studies of the postmortem specimens, to understand the mechanisms and improve the methodology.

Radiosurgery with Osvaldo Betti [62] Similarly, the Swedish school, led by Lars Leksell, combined stereotaxy and external radiotherapy to deliver high ionizing radiation with the precise doze in a well-defined spot. They developed the Gamma knife, made of several cobalt 60 sources, with convergent collimated beams on a determined point in space within the stereotactic frame. Initially designed to be applied in neurosurgery for movement disorders, this method has reached its full development in the treatment of arterio-venous malformations, improving the surgical outcome and reducing morbidity. More recently, this radiosurgery (which creates a lesion by radionecrosis) has been applied to tumors of small diameters and particularly to multiple brain metastases. In order to make this radiosurgery more accessible without being obliged to purchase the expensive Gamma knife system, the Talairach school, through its Argentinian pupil, Osvaldo Betti, has designed another instrument for radiosurgery using a linear accelerator, which he named LINAC. The stereotactic principles are satisfied by a physical connection between the linear accelerator and a chair rocking in two dimensions and to which the stereotactic frame is

History of stereotactic surgery in france

attached. The system has been installed at Hospital Tenon in Paris and became the first radiosurgical set-up used in France.

Harvesting the Crop When the Seeds Have Been Spread: The Development of Epilepsy Surgery Through Deep EEG Recording, Extended to Brain Tumor Surgery Jean Talairach, Jean Bancaud, Gabor Szikla, and Claudio Munari created a huge momentum in Sainte Anne, a school like which there are few in the world, and which could be compared to what happened at McGill around Penfield and Jasper. Most of the French stereotactic and functional neurosurgeons came here to be trained, and returned to Lille, Marseille, Grenoble, Rennes, Toulouse and Bordeaux, and later to other academic centers. Those who were to become famous in other parts of the world also visited Talairach’s school, learnt from it and also shared their knowledge, expertise and ideas. They came from and returned to Japan, Spain, Argentina, USA and Canada. Talairach had been trained in the Neurosurgery Department of Sainte Anne Hospital, under the supervision of his mentor, M. David. Since 1946, he had been developing stereotactic approaches to functional neurosurgery for chronic pain, movement disorders, pituitary diseases, and unoperable tumors. His interest was especially focused on the stereotactic definition of deep brain structures and he built up a coordinate system based on the anterior commissure-posterior commissure axis, which allowed him to “normalize” anatomical data from several brains. This led to the publication, in 1957, of his first stereotactic atlas on deep brain nuclei. His second stereotactic atlas, devoted to telencephalic structures, would be published 10 years later while he was already working with J. Bancaud. J. Bancaud, a neurologist

9

and electroencephalographer, was a student of H. Fishgold, a radiologist who was working at La Salpe´trie`re Hospital in Paris. At the beginning of the 1950s, Fishgold’s group joined David’s group in Sainte-Anne Hospital, and this undoubtedly represented a turning point for both Talairach and Bancaud’s careers. They were then gaining experience at the same institution, where epilepsy surgery had began, and they benefited from the high scientific experience of P. Buser and M.D. Dell in neurophysiology, and of H. Hecaen and J. de Ajurriaguera in neuropsychology. Bancaud saw the potential of Talairach’s method to localize the sources of EEG discharges in three dimensional space, and he began working with him to develop applications of stereotactic functional exploration for presurgical evaluation of medically intractable epilepsies. An operating room dedicated to stereotactic neurosurgery was opened at Sainte-Anne Hospital in 1959, and the project to record epileptic seizures by means of stereotactically implanted intracerebral electrodes became a reality. The term StereoElectroEncephaloGraphy (SEEG) [63–68] would be coined in 1962 to describe this new method, which, for many reasons, was revolutionary in the field of epilepsy surgery: SEEG recordings allowed the study of spatiotemporal dynamics of seizure discharges with respect to their clinical features, with a high degree of anatomical precision. The technique of SEEG offered the possibility to dissociate the presurgical investigation phase from the surgical therapeutic act: SEEG recordings and electrical stimulations were carried out in the operating room under “acute” conditions; after removal of the intracerebral electrodes, resection surgery was planned, and performed as a second step. SEEG was directly derived from a new conceptual approach for studying partial epileptic seizures, which was based on the assumption that the chronological occurrence of ictal clinical signs reflects the spatio-temporal organization of the epileptic

103

104

9

History of stereotactic surgery in france

discharge within the brain. The same year, Talairach’s team was joined by G. Szikla (1928–1983), an emigrant from Hungary where he had worked with Prof Zoltan, and who devoted his career to anatomy and stereotaxy, and played a major role in the development of stereotactic angiography. More particularly, carefully looking at the close relationships of cortical vessels to the gyri and sulci, Szikla showed that a meticulous analysis of vascular trajectories allowed the extraction of gyral form and dimension, and provided constant landmarks for the interpretation of anatomical variablity. Thus, stereotactic angiography was not only a routine procedure for safe implantation of intracerebral electrodes, but also a valuable tool for deducing the actual location of electrode contacts, particularly before the availability of modern imaging methods. The selection of the structures to be explored was based on a very careful analysis of all the data – notably clinical – collected during the non-invasive presurgical investigations. Such an analysis led to one or several hypotheses concerning the site(s) of seizure onset and the pathways of preferential ictal spread. Electrodes were then placed accordingly, in a way that enabled interpolation of intracerebral EEG activity within the interelectrode space. Proceeding this way, Bancaud and Talairach could precisely study how symptoms accumulated as the epileptic discharge propagated into different cortical structures and, in turn, could confirm or inform their initial hypotheses. The high spatial and temporal resolution, coupled with a high power of localization that the SEEG procedures offered, rapidly provided a large amount of data that had immediate repercussions on the practice of epilepsy surgery. This was mainly oriented towards tailored brain resection, but other avenues were not neglected. Deep brain stimulation for epilepsy in the thalamus (unpublished data) was initiated, following Mondragon and Lamarche’s work [69] on monkeys at Sainte Anne in Talairach’s INSERM unit U97, and this was the beginning of the application of STN stimulation to intractable nonoperable epilepsies

[70,71], in the wake of deep brain stimulation for movement disorders.

The Evolution of the Stereotactic Treatment of Movement Disorders The relation between stereotaxy and the treatment of movement disorders is the most exemplary as their mutual developments have been constantly linked during the last 50 years, in North America as well as in Europe, and particularly in France. In 1950, pallidotomies and ansotomies were performed in France by Fenelon [25,26], Guiot [27] and Gros [28] and by Mazars [72–80] through coagulation of the deep brain target through procedures guided on intraoperative visual landmarks. However, this procedure lacked precision and reliability, and the stereotactic approach was the logical next step. This step was taken by Guiot in France in 1952 [11], and quickly followed by Hassler and Riechert in Germany [81], Leksell in Sweden [82], Gillingham in Scotland [83], and Cooper [84,85] in the US as well as in Japan [86–88]. The lack of medical treatments for Parkinson’s disease, and even more for essential tremor, did no’t provide an alternative to the surgical treatment, which at that time was essentially ablative (microcoagulation, thermolesion, alcohol injection, or isotope insertion). Despite recurrences and complications, and because of its overall efficiency, the treatment of movement disorder remained the main condition for stereotaxy, until the advent of the levodopa era in the late 1960s. Since then, in France as well as in most of the Western countries, the surgical treatment of movement disorders, and therefore stereotaxy, underwent a dramatic decline, a few thalamotomies and pallidotomies still being performed in a limited number of expert centers. When, on the contrary, it appeared that some forms of Parkinson’s disease did not respond to the drugs or were plagued by motor

History of stereotactic surgery in france

fluctuations and dyskinesias, there was a new need for surgery. However, complications were unacceptable at that time and the method was required to evolve towards new directions, where efficacy would result in negligible morbidity. This led eventually to new developments such as brain grafting or, more recently, high frequency deep brain stimulation. Stereotaxy, like other methods, has experienced this type of fluctuation in its history and has on each occasion progressed and acquired new skills and possibilities, far beyond what it was initially designed for modern stereotactic surgery. The observation that after the honeymoon, levodopa had side effects such as levodopa-induced dyskinesias, and dopamine agonists induced hallucinatory and psychotic side effects, re-created the need for surgery and for new approaches. The saga of the brain grafts [89–92] did not involve French stereotaxy until the late 1990s when Marc Peschanski’s team [93–110], under a consensual but unspoken nationwide agreement, was considered as the only French team to engage in this difficult and highly skilled adventure. Since that period, he has contributed significantly to the advancement of the field of neural grafts, necessarily associated with the gene therapy domain [93,95,107,110]. He has applied this approach to movement disorders such as Parkinson’s disease, but mainly to Huntington’s disease [93– 96,100,101,103,106], which currently has no treatment. This is a clear example that some very specific fields of research and their applications should be totally assigned to a group, avoiding a sterile spread of financial and technical support. It was the reintroduction of Leksell’s pallidotomy by his two pupils Laitinen and Hariz in 1992 [111], and the introduction in 1987 of high frequency stimulation (HFS) [39–41,44,112– 114], that reinstalled in France, stereotaxy as an armamentarium of movement disorders. Its flexibility, adaptability, reversibility, and low morbidity, which help in performing HFS bilaterally,

9

have justified the quick and large development of this method in France, where the functional neurosurgery community and the neurologists, forming multidisciplinary teams, convinced the government to provide full reimbursement to this method. This allowed the development of several academic centers (up to 17 in 2007), and the extension to other movement disorders such as essential tremor and dystonia, to other targets than the Vim thalamus, such as the Pallidum and the subthalamic nucleus.

Stereotactic Surgery for Pain and the Development of Deep Brain and Cortical Stimulations Cancer pain was the most frequent indication of stereotaxy, particularly in the 1950s [115]. In the 1960s, Gabriel Mazars, also at Sainte Anne hospital in Paris, elaborated on the neurophysiological bases which were different from the gate control theory, a model of sensory perception and pain generation, on the basis of which he aimed at the thalamus and implanted electrodes [17–24], which were sometimes connected to an implantable stimulator, which was made on his ideas and then commercialized by the ELA company. At the same time in France several teams, sometimes in cooperation with other European countries [116], performed thalamic stimulation or periacqueductal gray (PAG) stimulation. Following the reports of the gate control theory by Wall and Melzack (1960), of the positive effects of thalamic stimulation for deafferentation pain and of the PAG for nociceptive pain, pain surgery also took advantage of the fundamental work of the INSERM team of Jean Marie Besson and Gise`le Guilbaud, which was close to Sainte Anne hospital. Quite often the practitioners of stereotactic surgery were very active in the field of functional neurosurgery as a whole and did not dissociate their activity from other methods such as spinal cord stimulation, for instance.

105

106

9

History of stereotactic surgery in france

This practice of deep brain stimulation for pain occurred in parallel to the large practice of spinal cord stimulation, which is not truly stereotactic, but part of functional neurosurgery. One must also mention Sedan in Marseille, Lazorthes in Toulouse, and Blond in Lille, who were very active in spinal cord stimulation as well as in intrathecal morphine, in strong correlation with the neurophysiologists. This created a real pain culture, which had a strong influence on the French stereotactic community, by calling for a more scientific approach, a critical evaluation of the results, and an ethical look at the overall field. In this stream of activity to try to treat pain, the work of Tsubokawa and his first reports on the efficiency of motor cortex stimulation for various types of pain, such as postherpetic facial pain or post-stroke (mainly thalamic) pain [117], attracted the attention of the teams led by Yves Keravel in Creteil Mondor Hospital [118], Marc Sindou in Lyon [119] and Yves Lazorthes in Toulouse [120].

The Introduction of Robotics and the Emergence of Neuronavigation in Stereotactic Surgery The quest for precision, reliability and safety never ends and takes advantage of all the available means. The logical extention of stereotaxy, increasingly based on numerical data provided by modern imaging, is to use these digital data to visualize targets on the MRI and CTscan modalities, to provide the possibility to draw trajectories and to plan procedures: this is what neuronavigation has progressively achieved in parallel to the increasing power of computers. The existence in Grenoble of industrial developments in the field of robotized multipurpose tools has naturally led to the concept, design and construction of a robotized stereotactic arm (Neuromate1 Schaerer-Mayfield, see chapter 37 in this

Handbook) [121] following the approaches of Kelly (a former fellow of J Talairach) [122] and of Ronald Young [123], aimed at replacing the grids, arch and goniometers of the stereotactic frame (ref Robots). In the same line of thought, a robotized microscope holder (Surgiscope1, ISIS) has been designed and built. These systems have been installed in several centers and are being currently routinely used and improved upon.

The Development of New Applications of Deep Brain Stimulation at High Frequency and the Rebirth of Psychosurgery in France New Applications of HFS Since the success of HFS in the treatment of Parkinson’s diseases, it has been extended to other targets (Vim, Pallidum, STN, CM-Pf) and also to other movement disorders (essential tremor, dystonia, tardive dystonia), based on the example of STN, which was derived from basic science. Other teams, in Italy, Belgium, and the Netherlands have successfully extended it to cluster headaches, obsessive compulsive disorders (OCD), and Tics de Gilles de la Tourette. In France, the fortuitous observation of the improvement by STN HFS of OCD symptoms in parkinsonian patients [124], led to the initiation of a multicenter clinical trial which has been successful in establishing the limbic portion of STN as a specific target for OCD treatments. This has been possible after the approval of the National Ethics Committee, an appeal to which was filed in December 2000 and which gave conditional approval in June 2002, for a carefully controlled clinical multicentric trial, similar to what happened in movement disorders, due to the growing interest in new indications. Psychosurgery had been almost stopped since the early 1970s in France, as a consequence of

History of stereotactic surgery in france

international pressure in the face of the abuses and complications, mainly lobotomies, even when stereotactic leucotomies were considered. There was in France very reduced psychosurgical stereotaxic activity in parallel to the development of the biological psychiatry and psychotherapy. There is now a new trend to return to psychosurgery for Tics and for depression, but the French neurosurgical community is very careful about the risks of jeopardizing one more time the possibility to help mental disorders if mistakes are made again.

Coma and Minimally Conscious States Franc¸ois Cohadon (1993) in Bordeaux, took a very careful and cautious approach to the problem of persisting vegetative post-traumatic states [125,126], at the same time as Tsubokawa [127,128] in Japan. In 25 cases of post traumatic vegetative state persisting 3 months after the initial injury, deep brain stimulation at low frequency has been used to activate the cortex with the hope of producing some degree of functional recovery. Electrodes were stereotactically implanted in the centrum medianum-parafascicularis complex. Bipolar stimulation was provided daily from 8 a.m. to 8 p.m. In 12 cases no changes occurred in the clinical features and overall behavior. DBS was given up after 2 months. All these patients with a follow-up of 1–10 years, remained in a permanent vegetative state, four of them eventually died. In 13 cases, following 1–3 weeks of DBS, a definite improvement was obtained with the recovery of some degree of consciousness and interpersonal relationship. Although some degree of long-term spontaneous recovery was documented, it was concluded that there was no significant effect. The reason why Cohadon, as well as Tubokawa, did not observe the results reported by Schiff et al. might be due to the fact that their patients were truly in vegetative states and not minimally conscious.

9

Conclusion French stereotaxy has reached a very internationally competitive level. Although one might consider that the first stereotactic frame was invented and used in 1897, stereotaxy seemed to start in the 1950s. Through two giant pioneers, it introduced multidisciplinarity as a philosophy. The group of Sante Anne created a whole monument of stereotactic discipline, which was wisely applied to several fields and created several approaches and strategies, developed atlases and frames, and inspired many young surgeons and students. French stereotaxy has remained very innovative since then. This was possible because stereotactic functional neurosurgery was and remained almost exclusively academic, was multidisciplinary with the primary goal of excellence, strong ethical concern and patient’s care, free from financial goals and economic considerations, as the French social security system did not demand economic criteria (length of stay, cost-benefit).

References 1. Horsley V, Clarke RH. The structure and functions of the cerebellum examined by a new method. Brain 1908;31:45–124. 2. Remy M, Contremoulins M. Le chercheur de projectiles, L’Illustration1897;55423 3. Zernov DN. Encephalometer: device for estimation of parts of brain in human. Proc Soc Physicomed Moscow Univ 1889;2:70-80. 4. Altukhov NV. Encephalometric investigations of the brain relative to the age, sex and skull indexes. Moscow; 1891. 5. Picard C, Olivier A, Bertrand G. The first human stereotaxic apparatus: The contribution of Aubrey Mussen to the field of stereotaxis. J Neurosurg 1983;59:673-6. 6. Olivier A, Bertrand G, Picard C. Discovery of the first human stereotactic instrument. Appl Neurophysiol 1983;46:84-91. 7. Spiegel EA, Wycis HT, Marks M, et al. Stereotactic apparatus for operations on the human brain. Science 1947;106:349-50.

107

108

9

History of stereotactic surgery in france

8. Sedan R, Duparet R. Stere´ometre adaptable au cadre ste´re´otaxique de J Talairach. Neurochirurgie 1968;14: 577-82. 9. Fenelon F, Thiebaut F. Re´sultats du traitement neurochirurgical d’une rigidite´ parkinsonienne par intervention striopallidale unilate´rale. Rev Neurol 1950;83:280. 10. Fenelon F. Essai de traitement neurochirurgical du syndrome parkinsonien par intervention directe sur les voies extrapyramidales imme´diatement sous-striopallidales (anses lenticulaires). Rev Neurol 1950;83:580-5. 11. Guiot G Brion S.“[Neurosurgery of choreoathetosic and Parkinsonian syndromes].” Sem Hop 1952;28 (49):2095-9. 12. Guiot G, Hardy J, Albe-Fessard D. De´limitation pre´cise des structures sous-corticales et identification de noyaux thalamiques chez l’homme par l’e´lectrophysiologie ste´re´otaxique. Neurochirurgia 1962;5:1-18 13. Guiot G, Derome P, Trigo JC. Le tremblement d’attitude: indication la meilleure de la chirurgie ste´reotaxique. Presse Med 1967;75:2513-8 14. Petit-Dutaillis, D., MessimyR, et al. “[Effect of prefrontal leucotomy on the behaviour of a maniac].” Rev Neurol (Paris) 1950;82(1):57-60. 15. Gros C,Vlahovitch B.“[Hemispherectomies; neurophysiological considerations].” Rev Neurol (Paris) 1951;85 (6):482-4. 16. Gros C, Vlahovitch B, et al. “[Effects of prefrontal interventions (leukotomy, topectomy) on psychic and kinetic manifestations of Parkinson syndrome].” Sem Hop 1955;31(32):1831-2. 17. Mazars G, Roge´ R, Mazars Y. Re´sultats de la stimulation du faisceau spino-thalamique et leur incidence sur la physiopathologie de la douleur. Revue Neurol 1960;20:136-8. 18. Mazars G, Merienne L, Cioloca G. Stimulations thalamiques intermittentes antalgiques. Revue Neurol 1973;128(4):273-9 19. Mazars G, Merienne L, et al. “[Use of thalamic stimulators in the treatment of various types of pain].” Ann Med Interne (Paris) 1975;126(12):869-71. 20. Mazars G. Intermittent stimulation of nucleus ventralis posterolateralis for intractable pain. Surg Neurol 1975;4:93-5. 21. Mazars G, Merienne L, et al. “[Present state of pain surgery].” Neurochirurgie 1976;22 Suppl 1:5-164. 22. Mazars G, Merienne L, et al. “[Effects of so-called periaqueductal gray substance stimulation].” Neurochirurgie 1979;25(2):96-100. 23. Mazars G, Merienne L, Cioloca G. Control of dyskinesias due to sensory deafferentation by means of thalamic stimulation. Acta Neurochirurgica Suppl (Wien) 1980;30:239-43. 24. Merienne L, Mazars G. Modification du sche´ma corporel sous stimulation thalamique. A propos des stimulations thalamiques pour membre fantoˆmes douloureux. Neurochirurgie 1981;27:121-3.

25. Fenelon F. “[Neurosurgery of parkinsonian syndrome by direct intervention on the extrapyramidal tracts immediately below the lenticular nucleus. Communication followed by film showing patient before and after intervention].” Rev Neurol (Paris) 1950;83(5):437-40. 26. Fenelon F. Bilan de quatre anne´es de pratique d’une intervention personnelle pour maladie de Parkinson. Rev Neurol 1953;89:580-5. 27. Guiot G, Brion S. Traitement des mouvements anormaux pour la coagulation pallidale. Technique et re´sultats. Rev Neurol 1953;89:578-80. 28. Gros C, Vlahovitch B, et al. “[the “Target” Zone in the Surgery of Parkinson’s Disease (Study of a Series of 407 Stereotaxic Operations)].” Neurochirurgie 1964;10:413-26. 29. Talairach J, Tournoux P.“[Apparatus for hypophysial stereotaxis by nasal approach].” Neurochirurgie 1955;1(1):127-31. 30. Szikla G, Talairach J.“Coordinates of the rolandic sulcus and topography of cortical and subcortical motor responses to low frequency stimulation in a proportional stereotaxic system.” Confin Neurol 1965;26(3):471-5. 31. Szikla G, Bouvicr G, Hori T, Petrov V. Angiography of the human brain cortex. New York: Springer; 1977. 32. Talairach J, David M, Tournoux P, et al. Atlas d’anatomie stereotaxique des noyaux gris centraux. Paris: Masson; 1957. 33. Talairach J, Szikla G, Tournoux P, et al. Atlas d’anatomie stereotaxique du telencephale. Paris: Masson; 1967. 34. Talairach J, Tournoux P. Coplanar stereotaxic atlas of the human brain: 3-dimensional proportional system: an approach to cerebral imaging. Stuttgart: Thieme Medical Publishers; 1988. 35. Albe-Fessard D, Arfel G, Guiot G, et al. De´rivation d’activite´s spontane´es et e´voque´es dans les structures ce´re´brales profondes de l’homme. Rev Neurol 1962;2:89-105. 36. Albe-Fessard D, Arfel G, Guiot G. Activite´s ´electriques caracte´ristiques de quelques structures ce´re´brales chez l’homme. Ann Chir 1963;17:1185-214. 37. Talairach J, Hecaen H, David M, et al. Recherches sur la coagulation the´rapeutique des structures sous-corticales chez l’homme. Rev Neurol 1949;81:4-24. 38. Talairach J, Tournoux P, Szikla G, et al. Traitement de la maladie de Parkinson: remarques me´thodologiques et technique chirurgicale. Gaz Med 1961;2:76-91. 39. Benabid A, Pollak P, Louveau A, et al. Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson’s disease. Appl Neurophysiol 1987;50:344-6. 40. Benabid A, Pollak P, Gervason C, et al. Long term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 1991;337:403-6. 41. Benabid A, Pollak P, Gao D, et al. Long term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. J Neurosurg 1996;84:203-14. 42. Blond S, Caparros-Lefebvre D, Parker F. Control of tremor and involuntary movement disorders by chronic

History of stereotactic surgery in france

43.

44.

45.

46.

47.

48.

49.

50.

51.

52.

53.

54. 55.

56.

57. 58.

stereotactic stimulation of the ventral intermediate thalamic nucleus. J Neurosurg 1992;77:62-8. Caparros-Lefebvre D, Blond S, Vermersch P, et al. Chronic thalamic stimulation improves tremor and levodopa induceddyskinesias in Parkinson’s disease. J Neurol Neurosurg Psych 1993;56:268-73. Limousin P, Pollak P, Benazzouz A, et al. Effect on Parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation.Lancet 1995;345(8942):91-5. Siegfried J. Effets de la stimulation du noyau sensitif du thalamus sur les dyskine´sies et la spasticite´. Rev Neurol (Paris) 1986;142:380-3. Siegfried J, Lippitz B. Chronic electrical stimulation of the globus pallidus in Parkinson’s disease. Acta Neurochir 1993;124:14-18. Tasker RR. Effets sensitifs et moteurs de la stimulation thalamique chez l’homme. Applications cliniques. Rev Neurol (Paris) 1986;142:316-26. Adams J, Hosobuchi Y, Fields H. Stimulation of internal capsule for relief of chronic pain. J Neurosurg 1974;41:740-4. Hosobuchi Y, Adams J, Rutkins B. Chronic thalamic stimulation for the control of facial anesthesia dolorosa. Arch Neurol 1973;29:158-61. Talairach J, deAJ, et al. “[Therapeutic sub-cortical coagulations; topographic study of the ventricular system in relation to the central gray nuclei].” Presse Med 1950;58 (38):697-701. Talairach J, De Aljuriaguerra J, et al. “[A stereotaxic study of the deep encephalic structures in man; technic; physiopathologic and therapeutic significance.].” Presse Med 1952;60(28):605-9. Talairach J. “[Destruction of the anterior ventral thalamic nucleus in the treatment of mental diseases].” Rev Neurol (Paris) 1952;87(4):352-7. Talairach J, Tournoux P.“[Stereotaxic localization of central gray nuclei].” Neurochirurgia (Stuttg) 1958;1(1): 88-93. Talairach J, Tournoux P, et al. “[Parietal surgery of pain].” Acta Neurochir (Wien) 1960;8:153-250. Talairach J, Ruggiero G, et al. “A new method of treatment of inoperable brain tumours by stereotaxic implantation of radioactive gold; a preliminary report.” Br J Radiol 1955;28(326):62-74. Talairach J, Szikla G, et al. “[Stereotaxic destruction of the nontumoral hypophysis by radioactive isotopes. (Hypophysectomy for hormone-dependent cancer. Interstitial radiotherapy for malignant exphthalmos and Cushing’s syndrome of high origin)].” Presse Med 1962;70:1399-402. Talairach J, Szikla G, et al. “[Pituitary sterotaxic surgery].” Confin Neurol 1962;22:204-16. Talairach J, Bonis A, et al. “[Technic and results of interstitial radiotherapy of the pituitary in various endocrine syndromes: chromophobe adenoma, acromegaly and Cushing’s disease].” Acta Isot (Padova) 1964;4(4):355-85.

9

59. Talairach J, Szikla G.“[Amygdalo-hippocampal partial destruction by yttrium-90 in the treatment of certain epilepsies of rhinencephalic manifestation].” Neurochirurgie 1965;11(3):233-40. 60. Talairach J Szikla G.“[Intrasellar application of radioactive isotopes from a functional standpoint (mammary carcinoma, malignant, exophthalmos, Cushing’s syndrome, diabetes, malignant arterial hypertension)].” Nucl Med (Stuttg) 1965;:2:Suppl 371+. 61. Talairach J, Szikla G, et al. “Therapeutic utilization of radioactive isotopes in pituitary surgery.” Int J Neurol 1965;5(1):78-93. 62. Betti O, Derechinsky V.“[Multiple-beam stereotaxic irradiation].” Neurochirurgie 1983;29(4):295-8. 63. Bancaud J, Talairach J.“[Epilepsy of the supplementary motor area: a particularly difficult diagnosis in children].” Rev Neuropsychiatr Infant 1965;13(6):483-99. 64. Bancaud J, Talairach J.“[Methodology of stereo EEG exploration and surgical intervention in epilepsy].” Rev Otoneuroophtalmol 1973;45(4):315-28. 65. Talairach J, Bancaud J, et al. “[New approach to the neurosurgery of epilepsy. Stereotaxic methodology and therapeutic results. 1. Introduction and history].” Neurochirurgie; 19741:20 Suppl 1-240. 66. Talairach J, Szikla G.“Application of stereotactic concepts to the surgery of epilepsy.” Acta Neurochir Suppl (Wien) 1980;30:35-54. 67. Talairach J, Tournoux P, et al. “Stereotaxic exploration in frontal epilepsy.” Adv Neurol 1992;57:651-88. 68. Talairach J, Bancaud J, et al. “Surgical therapy for frontal epilepsies.” Adv Neurol 1992;57:707-32. 69. Mondragon S, Lamarche M.“Suppression of motor seizures after specific thalamotomy in chronic epileptic monkeys.” Epilepsy Res 1990;5(2):137-45. 70. Benabid AL, Minotti L, Koudsie A, de Saint Martin A, Hirsch E. Antiepileptic effect of high-frequency stimulation of the subthalamic nucleus (corpus luysi) in a case of medically intractable epilepsy caused by focal dysplasia: a 30-month follow-up: technical case report. Neurosurgery 2002;50(6):1385-91; discussion 1391-92. 71. Chabardes S, Kahane P, Minotti L, Koudsie A, Hirsch E, Benabid AL. Deep brain stimulation in epilepsy with particular reference to the subthalamic nucleus. Epileptic Disord 2002;4 Suppl 3:83-93. 72. MazarsMazars G. “[Surgical treatment of Parkinson’s disease].” Gaz Med Fr 1959;66(12):1063-4. 73. Mazars G, Droguet P, et al. “[Volitional dyskinesia of posture. Disappearance of the dyskinesia after thalamic coagulation].” Rev Prat 1960;103:73-4. 74. Mazars G, Pansini A, et al. “[Homolateral responses caused by stimulation of the radiating crown and of the internal capsule].” Rev Prat 1960;103:134-6. 75. Mazars G, Pansini A, et al. “[Contribution to the knowledge of the relations between the lesions produced by surgery of dyskinesias and the principal motor tract].” Rev Prat 1961;104:433-6.

109

110

9

History of stereotactic surgery in france

76. Mazars G, Chodkiewicz JP, et al. “[The cephalogyric contingent of the cortico-capsular fibers].” Rev Neurol (Paris) 1965;112(6):553-7. 77. Mazars G, Chodkiewicz JP, et al. “[Nosology and therapeutic indications in cervico-cephalic dyskinesias].” Rev Neurol (Paris) 1967;116(5):441-3. 78. Mazars G, Merienne L, et al. “[Surgery of cephalic orientation dyskinesia].” Neurochirurgie 1968;14(6):745-52. 79. Mazars G, Merienne L, et al. “[Dyskinesias of the upper limb associated with dyskinesias of cephalic orientation. Study of 45 cases and presentation of a film].” Rev Neurol (Paris) 1970;122(4):275-7. 80. Merienne L, Mazars G. Traitement de certaines dyskine´sies par stimulation thalamique intermittente. Neurochirurgie 1982;28:201-6. 81. Hassler R, Riechert T, Mundinger F, Umbach W, Ganglberger J. Physiological observations in stereotaxic operations inextrapyramidal motor disturbances. Brain 1960;83:337-51. 82. Svennilson E, Torvik A, Lowe R, et al. Treatment of parkinsonism by stereotactic thermolesions in the pallidal region. Acta Psychiatr Neurol Scand 1960;35:359-77. 83. Kelly PJ, Gillingham FJ. The long-term results of stereotacticsurgery and L-dopa therapy in patients with Parkinson’s disease. A 10-year follow-up study. J Neurosurg 1980;53:332-7. 84. Cooper IS, Bravo GI. Chemopallidectomy, and chemothalamectomy. J Neurosurg 1958;15:244-56. 85. Cooper IS. Surgical treatment of parkinsonism. Ann Rev Med 1965;16:309-30. 86. Narabayashi H, Okuma T. Procaine oil blocking of the globuspallidus for treatment of rigidity and tremor of parkinsonism:preliminary report. Proc Jpn Acad 1953;29:134. 87. Narabayashi H, Yokoshi F, Nakajiina Y. Levodopa induced dyskinesia and thalamotomy. J Neurol Neurosurg Psychiatr 1984;47:831-9. 88. Ohye C, Maeda T, Narabayashi H. Physiologically defined VIM nucleus: its special reference to control of tremor. AppliedNeurophysiol 1976;39:285-95. 89. Backlund E, Granberg P, Hamberger B, et al. Transplantation of adrenal medullary tissue to striatum in parkinsonism. First clinical trials. J Neurosurg 1985;62: 169-73. 90. Bjo¨rklund A, Stenevi U. Reconstruction of the nigrostriatal dopamine pathway by intracerebral nigral transplants. Brain Res 1979;177:555-60. 91. Bjo¨rklund A, Stenevi U, Dunnett S. Functional reactivation the deafferented neostriatum by nigral transplant. Nature 1981;289:497-9. 92. Bjorklund A, Dunnett SB, et al. “Neural transplantation for the treatment of Parkinson’s disease.” Lancet Neurol 2003;2(7):437-45. 93. Peschanski’s team Bachoud-Levi AC, Hantraye P, et al. “Prospectives for cell and gene therapy in Huntington’s disease.” Prog Brain Res 1998;117:511-24.

94. Bachoud-Levi AC, Remy P, et al. “Motor and cognitive improvements in patients with Huntington’s disease after neural transplantation.” Lancet 2000;356(9246):1975-9. 95. Bachoud-Levi AC, DeglonN, et al. “Neuroprotective gene therapy for Huntington’s disease using a polymer encapsulated BHK cell line engineered to secrete human CNTF.” Hum Gene Ther 2000;11(12):1723-9. 96. Bachoud-Levi AC, Gaura V, et al. “Effect of fetal neural transplants in patients with Huntington’s disease 6 years after surgery: a long-term follow-up study.” Lancet Neurol 2006;5(4):303-9. 97. Peschanski M, Rudin M, et al. “Magnetic resonance imaging of intracerebral neural grafts.” Prog Brain Res 1988;78:619-24. 98. Peschanski M, Defer G, et al. “Bilateral motor improvement and alteration of L-dopa effect in two patients with Parkinson’s disease following intrastriatal transplantation of foetal ventral mesencephalon.” Brain 1994;117 (Pt 3): 487-99. 99. Peschanski M. “The breaking of embargoes.” Lancet 2001;357(9260):963. 100. Peschanski M, Dunnett SB.“Cell therapy for Huntington’s disease, the next step forward.” Lancet Neurol 2002;1(2):81. 101. Peschanski M, Bachoud-Levi AC, et al. “Integrating fetal neural transplants into a therapeutic strategy: the example of Huntington’s disease.” Brain 2004;127 (Pt 6):1219-28. 102. Peschanski M. “[Stem cells, time for scale-up].” Med Sci (Paris) 2008;24(4):335-7. 103. Lefaucheur JP, Menard-Lefaucheur I, et al. “Electrophysiological deterioration over time in patients with Huntington’s disease.” Mov Disord 2006;21(9):1350-4. 104. Levivier M, Dethy S, et al. “Intracerebral transplantation of fetal ventral mesencephalon for patients with advanced Parkinson’s disease. Methodology and 6-month to 1-year follow-up in 3 patients.” Stereotact Funct Neurosurg 1997;69(1–4 Pt 2):99-111. 105. Mitjavila-Garcia MT, Simonin C, et al. “Embryonic stem cells: meeting the needs for cell therapy.” Adv Drug Deliv Rev 2005;57(13):1935-43. 106. Palfi S, Ferrante RJ, et al. “Chronic 3-nitropropionic acid treatment in baboons replicates the cognitive and motor deficits of Huntington’s disease.” J Neurosci 1996;16 (9):3019-25. 107. Peltekian E, Parrish E, et al. “Adenovirus-mediated gene transfer to the brain: methodological assessment.” J Neurosci Methods 1997;71(1):77-84. 108. Cesaro P, Peschanski M, et al. “Treatment of Parkinson’s disease by cell transplantation.” Funct Neurol 2001;16 (1):21-7. 109. Cochen V, Ribeiro MJ, et al. “Transplantation in Parkinson’s disease: PET changes correlate with the amount of grafted tissue.” Mov Disord 2003;18(8):928-32. 110. Bloch J, Bachoud-Levi AC, et al. “Neuroprotective gene therapy for Huntington’s disease, using

History of stereotactic surgery in france

111.

112.

113.

114.

115.

116.

117.

118.

polymer-encapsulated cells engineered to secrete human ciliary neurotrophic factor: results of a phase I study.” Hum Gene Ther 2004;15(10):968-75. Laitinen LV, Bergenheim AT, Hariz MI. Leksell’s posteroventral pallidotomy in the treatment of Parkinson’s disease. J Neurosurg 1992;76:53-61. Benabid AL, Pollak P, Gervason C, Hoffmann D, Gao DM, Hommel M, et al. Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 1991;337(8738): 403-6. Limousin P, Krack P, Pollak P, Benazzouz A, Ardouin C, Hoffmann D, et al. Electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med;1998;339(16):1105-11. Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, et al. Five years follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 2003;349:1925-34. Gros C, Vlahovitch B, et al. “[Personal experience with surgery of pain in cancer].” J Radiol Electrol Arch Electr Medicale 1955;36(7–8):618-20. Blond S, Siegfried J.“Thalamic stimulation for the treatment of tremor and other movement disorders.” Acta Neurochir Suppl (Wien) 1991;52:109-11. Tsubokawa T, Katayama Y, et al. “Chronic motor cortex stimulation for the treatment of central pain.” Acta Neurochir Suppl (Wien) 1991;52:137-9. Nguyen JP, Lefaucher JP, Le Guerinel C, Eizenbaum JF, Nakano N, Carpentier A, et al. “Motor cortex stimulation in the treatment of central and neuropathic pain.” Arch Med Res 2000;31(3):263-5.

9

119. Garcia-Larrea L, Peyron R. Motor cortex stimulation for neuropathic pain: From phenomenology to mechanisms.” Neuroimage 2007;37 Suppl 1:S71-9. 120. Lazorthes Y, Sol JC, Fowo S, Roux FE, Verdie JC. “Motor cortex stimulation for neuropathic pain.” Acta Neurochir Suppl 2007;97(Pt 2):37-44. 121. Benabid AL, Hoffmann D, Lavallee S, Cinquin P, Demongeot J, Lebas JF, et al. Is there any future for robots in neurosurgery? In: SymonL, editors. Advances and Technical Standards in Neurosurgery, vol. 18. Springer: Wien New York; p. 3-45 122. Kelly PJ, Alker GJ. A method for stereotactic laser microsurgery in the treatment of deep seated CNS neoplasms. Appl Neurophysiol 1980;43:210-15. 123. Young RJ. Application of robotics to stereotactic neurosurgery. Neurol Res 1887;9:123-8. 124. Mallet L, Mesnage V, et al. “Compulsions, Parkinson’s disease, and stimulation.” Lancet 2002;360(9342):1302-4. 125. Cohadon F,Richer E. “[Post-traumatic vegetative states].” Neurochirurgie 1993;39(5):269-80. 126. Cohadon F, Richer E. “[Deep cerebral stimulation in patients with post-traumatic vegetative state. 25 cases].” Neurochirurgie 1993;39(5):281-92. 127. Tsubokawa T, Yamamoto T, et al. “Deep-brain stimulation in a persistent vegetative state: follow-up results and criteria for selection of candidates.” Brain Inj 1990;4 (4):315-27. 128. Yamamoto T, Katayama Y, et al. “Deep brain stimulation therapy for a persistent vegetative state.” Acta Neurochir Suppl 2002;79:79-82.

111

4 History of Stereotactic Surgery in Germany J. K. Krauss

Stereotactic and functional neurosurgery has a long and rich history in Germany [1,2]. At the time functional and stereotactic surgery was introduced in clinical practice, medical progress had slowed down considerably during the post-World War II depression era. In this article, a brief overview on the pre-war development of neurosurgery in Germany with a special emphasis on issues relevant to functional neurosurgery, followed by a more thorough review on the birth of functional neurosurgery in Freiburg and its further achievements are discussed. The account is based on original historical documents, previous historical reviews and a personal interview, and the reader is referred to those documents for a more complete bibliography on this topic [1,3–6].

Development of Neurosurgery in Germany Ernst von Bergmann was the first German surgeon who devoted his career to surgery of the nervous system [7]. He became professor of surgery in 1878, in Wu¨rzburg, and he moved to the Charite´ in Berlin, in 1882. He published several books focussing on neurosurgical topics. When he died in 1907, several of his pupils continued to carry on his interests. The two major driving forces for the further development ultimately were Fedor Krause and Otfrid Fo¨rster [8,9]. Fedor Krause developed his career first in Hamburg, and later in Berlin. In February, 1892, he explored the trigeminal nerve via an extradural approach for treatment of trigeminal #

Springer-Verlag Berlin/Heidelberg 2009

pain. He was active in many other aspects of neurosurgery and was highly esteemed when he died in 1937. Otfrid Fo¨rster, who was 18 years younger than Krause, was the first to pioneer the concept that neurosurgery should be an independent discipline in Germany. Fo¨rster was trained as a neurologist and a neurophysiologist, but he was rather an autodidact in surgery. He became well known during the 1920s and had contacts with Bailey, Bucy, Penfield, and Cushing. Fo¨rster was invited to Moscow after Lenin suffered from an apoplectic insult. When Lenin died, it was he who signed the protocol of the autopsy reporting hemorrhage from an aneurysm of the medial cerebral artery. Fo¨rster furthered many innovations in neurosurgery at his institute in Breslau. He was the first to pioneer dorsal rhizotomy for treatment of spasticity, and cordotomy for treatment of pain syndromes. In 1937, when the sky was clouded already by the reign of the Nazi regime and the international reputation of Germany became more and more overshadowed, he still managed to organize a German-British meeting of neurosurgeons in Berlin and became a honorary member of the British neurosurgical society [9]. He died in 1940 at the age of 67. It was Wilhelm To¨nnis who became the first chair of an ‘‘extraordinariate’’ in 1937, in Berlin [10]. Although he is mostly known for his work on trauma surgery, he established fruitful contacts with other neurodisciplines including new concepts such as neuropathology. Spatz and Hallervorden were the first to describe more extensively the disorder which carried their names for decades and was renamed recently in neurodegeneration with brain iron accumulation [11].

54

4

History of stereotactic surgery in germany

The development of neurosurgery in Germany came to a sudden halt when World War II began [10]. When the war was over, neurosurgery soon became an advanced discipline, during the reorganization of healthcare, not devoted mainly to trauma anymore.

Freiburg: the Early Epicentre of German Functional and Stereotactic Neurosurgery Traugott Riechert, born in 1905, was a pupil of To¨nnis who had worked on brain injury during the Second World War. He was the second in Germany to become professor of neurosurgery on June 27, 1946, in Freiburg. At that time, psychiatry and neurology in Freiburg were united under the leadership of the psychiatrist Behringer. Richard Jung, who later became the head of the department of neurology, and Rolf Hassler, who established a laboratory for neuropathology, were members of the faculty. Hassler had come to Freiburg from Berlin after the war was over. He was a pupil of the internationally renowned scientists, Cecile and Oscar Vogt, who had to leave Berlin when the nazis had taken over, to be replaced by Spatz. The Vogts were actually the first to forge the term ‘‘extrapyramidal system.’’ When they left Berlin to move to the Black Forest, they brought with them a large collection of brains (among them was Lenin’s brain) and brain slices which was one of the reason that Rolf Hassler was also attracted to come to Freiburg. When Riechert accepted the call to Freiburg in 1946, he had no rooms available in his department [6]. Therefore, he was housed initially in an attic of the psychiatry department. In the late 1947, the department of neurosurgery assumed its operative activities after Watts had visited Freiburg to demonstrate the technique of Freeman and Watts to perform transorbital leucotomy. This procedure was performed on a few patients in Freiburg and interestingly treated intractable pain also, but it

never became popular. Riechert made rounds in the psychiatry ward, and every Saturday there was a big conference attended by the neurologists and psychiatrists. The first stereotactic frame in Freiburg was developed during this period by Riechert together with the physicist, Wolff [12]. It was quite inaccurate, but it was the prototype for the second model which became to be known as the Riechert-Mundiger frame [13]. When Richard Jung became the interim chair of the department of psychiatry after the death of Behringer, he asked the residents whether one of them would like to join the neurosurgeons [9]. Fritz Mundinger volunteered, and he started his career in neurosurgery in 1951. At that time Hassler had become the head of the neuropathology laboratory. Mundinger first concentrated on the improvement of the accuracy of the stereotactic frame and every afternoon, if possible, he met with the technician F. L. Fischer of the Fischer Company to develop the device further into the shape it later became known and still exists today [13]. Functional stereotactic neurosurgery in Freiburg started with pallidotomies [14]. While it became recognized that rigidity responded quite well to pallidotomy, it was also noted that tremor was ameliorated to a much lesser extent. Also, with the early lesioning systems, hemorrhages were not infrequent and they were thought to be partially related to the vascular supply of the pallidum. By that time Hassler was already known as ‘‘the expert of the thalamus’’ worldwide. He had managed to establish his own nomenclature dividing the thalamus into 34 subnuclei based on their cytoarchitectonic structures and their cortical and subcortical connections [3]. His classification was already published in his habilitation thesis in 1948. It was he who suggested to target the thalamus based on his neuroanatomic concepts, and also to stay out of trouble with the branches of the anterior choroidal artery during pallidotomy. He argued that it would be useful not only to target the pallidothalamic system, but also the dentatothalamic system and their projections to

History of stereotactic surgery in germany

the cortex. He thought that the ventralis oralis anterior nucleus would be a good target for rigidity, and hence he suggested the ventralis oralis posterior nucleus as an ideal target for tremor. The basic problem, however, was to identify and find the nuclei. The time had come to introduce thalamotomy for treatment of movement disorders. The first thalamotomy ever was actually performed on November 14, 1952, in Freiburg [15]. The patient was a 38-year-old man with postencephalitic parkinsonism with prominent tremor. The target coordinates were determined by comparing the pneumencephalography X-rays, which were made several days prior to the operation with 5 mm brain slices that Hassler had prepared. The algorithm for target calculation taking into account cranio-cerebral correlations and X-ray distortion was quite complicated. The operation was performed by Mundinger in the presence of Riechert, Hassler, and von Baumgarten. The immediate result was that the tremor stopped and the response of both, the patient and the physicians, was overwhelming. The results were published two years later in 1954, by Hassler and Riechert, in German, in ‘‘Der Nervenarzt’’ [15]. Over the next few years, pallidotomy was replaced step-by-step by thalamotomy in Freiburg. Subsequently, Freiburg became the first major center for stereotactic and functional neurosurgery in Germany. In 1960, thousands of functional stereotactic procedures had been performed in the department [16,17]. Over the next few years, the department became extremely busy and up to five thalamotomies for Parkinson’s disease were performed each day. Also, the indications were expanded and other movement disorders such as dystonia, myoclonus, hemiballism, and tics were successfully treated by thalamotomies [18–22]. In the early 1960s, the zona incerta was introduced as a target for ablative surgery [23]. With the development of temperature control and radiofrequency lesioning, lesions could now be made much smaller and side effects were significantly

4

reduced [24,25]. The effects of both low frequency and high frequency stimulation with electric current via the radiofrequency probe were studied systematically as early as in the late 1950s [26,27]. Another early development in Freiburg was the use of radionuclides to treat brain tumors [6]. In 1951, the first radionuclide used was phosphor 32. Later the most frequently used radionuclides were iodine 125 and iridium 192. During the 1950s, stereotactic implantation of radionuclides was used in the treatment of movement disorders in 20 patients. In 1963, Mundinger developed the ‘‘Gammamed’’ for brachyradiotherapy [4]. This machine was constructed for high-dose radiation and it was loaded with iridium 192. Radiation therapy was delivered by stereotactic techniques.

Spread Over Germany While the department of neurosurgery in Freiburg grew and became larger, many visitors and several guests from Germany and other countries (> Figure 4-1) were trained there in functional stereotactic neurosurgery. Many of them spread the technique to other cities, were they worked in the frame of general neurosurgery or in specialized subunits. Some of them were: Dieckmann in Homburg, Umbach in Berlin, Spuler in Wu¨rzburg, Mu¨ller in Hamburg, Thomalske in Frankfurt, Nittner in Cologne, and Yasargil in Zurich [28]. Independent departments for stereotactic and functional neurosurgery were built in Freiburg, Homburg, Frankfurt, and Wu¨rzburg. Many of these neurosurgeons modified the stereotactic techniques they had learned in Freiburg and expanded the indications. Struppler, who became active over decades in Munich, actually was trained as a neurologist. When Germany was divided into two countries, there was little cross-border exchange due to the restrictions of the cold war. Nevertheless, Goldhahn managed to establish functional stereotactic neurosurgery in Leipzig,

55

56

4

History of stereotactic surgery in germany

. Figure 4-1 Mundlinger (second from left) and Riechert (third from left) at the entrance of the building which housed the neurosurgical department in Freiburg in the 1960s together with guests from Russia including Ugrumov (third from right)

East Germany (formerly communist ‘‘Deutsche Demokratische Republik’’) [29]. The first major atlas for stereotactic surgery of the human brain ‘‘Stereotaktische Operationen/ Stereotaxis’’ was edited by Georges Schaltenbrand from Wu¨rzburg and by Percival Bailey from Chicago [30]. It was published in three volumes by Georg Thieme Verlag, Stuttgart, in 1959. This atlas had a major impact on the further development of functional stereotactic surgery. Strong input into the atlas was supplied by Hassler, Riechert, and Mundinger, and its development was also supported by Leksell. Twenty years later its second edition ‘‘The Atlas for Stereotaxy of the Human Brain’’ was published, this time edited by Georges Schaltenbrand and Waldemar Wahren

[31]. While the first edition ‘‘The Schaltenbrand/ Bailey Atlas’’ was bilingual – German and English, the second edition ‘‘The Schaltenbrand/Wahren Atlas’’ was only in English. Tragically, after writing the foreword to the accompanying textbook edited by Schaltenbrand and Walker [32], Schaltenbrand suffered a stroke and died before the second edition of his monumental work went to press. While there was a strong focus on functional stereotactic neurosurgery for treatment of movement disorders in Germany, other classical indications like pain, psychoaffective disorders, and epilepsy were developed further. As indicated above, classical leucotomy did not have a wide distribution in Germany. Also, after the introduction of stereotactic techniques to target subcortical

History of stereotactic surgery in germany

4

structures for psychoaffective disorders, psychosurgery was rather limited and such procedures were confined to six centers [33]. As in other countries, psychosurgery came to a complete halt in the 1970s, when it came to the focus of public attention and provoked overwhelmingly unwanted responses in the media.

Charite in ‘‘East’’ Berlin [36]. The revival of movement disorders surgery in Germany was closely related to the introduction of deep brain stimulation [37]. The base for treatment of movement disorders is now widely distributed all over Germany with major centers in Freiburg, Cologne, Berlin, Magdeburg, Kiel and Hannover.

Silent Years and Revival

References

Birkmayer and Hornykiewicz had already published their observations on levodopa in parkinsonism in 1961, in a German journal [34]. After the general introduction of levodopa in clinical practice in the late 1960s, the number of functional stereotactic procedures for treatment of Parkinson’s disease sharply dropped, and over the years many centers completely stopped their activities. Nevertheless, some institutions still remained active. Even when thalamotomy had become completely out of public focus, about 100 thalamotomies were performed each year for treatment of tremor or Parkinson’s disease. When I joined Mundinger in the department of functional and stereotactic neurosurgery as a resident, in Freiburg, in 1988, I had the unique opportunity to learn this procedure. The academic interest in functional and stereotactic neurosurgery was always strong in Germany. During the 1960s and the 1970s networks with colleagues from other European countries became more and more apparent. As detailed in chapter A2 the founding meeting of the European Society of Stereotactic and Functional Neurosurgery was in Freiburg in 1970. While pallidotomy became a major procedure for treatment of movement disorders in the United States and in several European countries after Laitinen had raised it from oblivion [35], it became never really popular in Germany. Also, partially for legal reasons neurotransplantation never had a more widespread application in the 1980s and 1990s with the exception of some patients having been operated on by Vogel in the

1. Krauss JK, Grossmann RG. Historical review of pallidal surgery for treatment of parkinsonism and other movement disorders. In: Krauss JK, Grossmann RG, Jankovic J, editors. Pallidal surgery for the treatment of Parkinson’s disease and movement disorders. Philadelphia: LippincottRaven; 1998. p. 1-23. 2. Sturm V. Stereotaxie. In: Arnold H, et al., editors. Neurochirurgie in Deutschland: Geschichte und Gegenwart. Berlin, Wien: Blackwell; 2001. p. 254-7. 3. Hassler R, Mundinger F, Riechert T. Stereotaxis in Parkinson syndrome. Berlin, Heidelberg, New York: Springer; 1979. 4. Mundinger F. Stereotaktische Operationen am Gehirn. Stuttgart: Hippokrates; 1975. 5. Riechert T. Stereotactic brain operations. Bern, Stuttgart, Vienna: Huber; 1980. 6. Krauss JK. Interview with Professor Mundinger. AANS Archives Video Interview series: Leaders in Neuroscience; 1998. 7. Bushe KA, Collmann H. Neurochirurgie von den Anfa¨ngen bis zum spa¨ten 19. Jahrhundert. In: Arnold H, et al., editors. Neurochirurgie in Deutschland: Geschichte und Gegenwart. Berlin, Wien: Blackwell; 2001. p. 1-23. 8. Collmann H, Halves E, Arnold H. Neurochirurgie in Deutschland von 1880 bis 1932. In: Arnold H, et al., editors. Neurochirurgie in Deutschland: Geschichte und Gegenwart. Berlin, Wien: Blackwell; 2001. p. 25-77. 9. Frowein RA, Dietz H, Rosenow DE, Vitzthum HE. Neurochirurgie in Deutschland von 1932 bis 1945. In: Arnold, H, et al., editors. Neurochirurgie in Deutschland: Geschichte und Gegenwart. Berlin, Wien: Blackwell; 2001. p. 79-95. 10. Frowein RA, Dietz H, Franz K. Neurochirurgie in Deutschland von 1945 bis 1970, In: Arnold H, et al., editors. Neurochirurgie in Deutschland: Geschichte und Gegenwart. Berlin, Wien: Blackwell; 2001. p. 97-119. 11. Thomas M, Hayflick SJ, Jankovic J. Clinical heterogeneity of neurodegeneration with brain iron accumulation (Hallervorden-Spatz syndrome) and pantothenate kinase-associated neurodegeneration. Mov Disord 2004;19:36-42.

57

58

4

History of stereotactic surgery in germany

12. Riechert T, Wolff M. Die technische Durchfu¨hrung von gezielten Hirnoperationen. Arch Psychiat Zeitschr Neurol 1953;190:297-316. 13. Riechert T, Mundinger F. Beschreibung und Anwendung eines Zielgera¨tes fu¨r stereotaktische Hirnoperationen (II. Modell). Acta Neurochir 1956;3:308-37. 14. Mundinger F, Riechert T. Ergebnisse der stereotaktischen Hirnoperationen bei extrapyramidalen Bewegungssto¨rungen auf Grund postoperativer und Langzeituntersuchungen. Dtsch Ztschr Nervenheilk 1961;182:542-76. 15. Hassler R, Riechert T. Indikationen und Lokalisationsmethode der gezielten Hirnoperationen. Nervenarzt 1954;25:441-7. 16. Mundinger F, Riechert T. Die stereotaktischen Hirnoperationen zur Behandlung extrapyramidaler Bewegungssto¨rungen (Parkinsonismus und Hyperkinesen) und ihre Resultate. Fortschr Neurol Psych 1963;31:1-66, 69-120. 17. Mundinger F, Riechert T. Indikationen und Langzeitergebnisse von 1400 uni- und bilateralen stereotaktischen Eingriffen beim Parkinsonsyndrom. Wien Zschr Nervenhk 1966;23:147-77. 18. Riechert T. The stereotactic technique and its application in extrapyramidal hyperkinesia. Confin Neurol 1972;34:325-30. 19. Mundinger F, Riechert T, Disselhoff J. Long-term results of stereotactic treatment of spasmodic torticollis. Confin Neurol 1972;34:41-6. 20. Mundinger F, Riechert T, Disselhoff J. Long term results of stereotaxic operations on extrapyramidal hyperkinesia (excluding parkinsonism). Confin Neurol 1970;32:71-8. 21. Krauss JK, Mundinger F. Functional stereotactic surgery for hemiballism. J Neurosurg 1996;85:278-86. 22. Loher TJ, Pohle T, Krauss JK. Functional stereotactic neurosurgery for treatment of cervical dystonia: review of the experience from the lesional era. Stereotact Funct Neurosurg 2004;82:1-13. 23. Mundinger F. 30 Jahre stereotaktische Hirnoperationen beim Parkinsonismus (Ergebnisse im Vergleich pallidosubthalamischer Ausschaltungen und Indikationen). In: Ga¨nshirt H, Berlit P, Haack G, editors. Pathophysiologie, Klinik und Therapie des Parkinsonismus. Basel: Editiones Roche; 1983. p. 331-57.

24. Gross I. Klinische Vergleichsuntersuchungen zwischen der konventionellen und der frequenzreinen, temperaturkontrollierten Hochfrequenzkoagulation zur stereotaktischen subkortikalen Ausschaltung. Inaugural Dissertation. Albert-Ludwigs-Universita¨t, Freiburg, 1964. 25. Hassler R, Mundinger F, Riechert T. Correlations between clinical and autoptic findings in stereotactic operations of parkinsonism. Confin Neurol 1965;26:282-90. 26. Hassler R, Riechert T. Wirkungen der Reizungen und Koagulationen in den Stammganglien bei stereotaktischen Hirnoperationen. Nervenarzt 1961;32:97-109. 27. Hassler R, Riechert T, Mundinger F, Umbach W, Ganglberger JA. Physiological observations in stereotaxic operations in extrapyramidal motor disturbances. Brain 1960;83:337-54. 28. Krayenbu¨hl H, Wyss OAM, Yasargil MG. Bilateral thalamotomy and pallidotomy as treatment for bilateral parkinsonism. J Neurosurg 1961;18:429-44. 29. Goldhahn G, Goldhahn WE. Experience with stereotaxic brain surgery for spasmodic torticollis. Zentralbl Neurochir 1977;38:87-96. 30. Schaltenbrand G, Bailey P. Introduction to stereotaxis with an atlas of the human brain. Stuttgart: Thieme; 1959. 31. Schaltenbrand G, Wahren W. Atlas for stereotaxy of the human brain. Stuttgart: Thieme; 1977. 32. Schaltenbrand G, Walker EA. Stereotaxy of the human brain. Stuttgart, New York: Thieme; 1982. 33. Mu¨ller D. Psychiatrische Chirurgie (sog. Psychochirurgie). In: Arnold, H, et al., editors. Neurochirurgie in Deutschland: Geschichte und Gegenwart. Berlin, Wien: Blackwell; 2001. p. 258-66. 34. Birkmayer W, Hornykiewicz O. Der L-Dioxyphenylalanin (L-Dopa)-Effekt bei der Parkinson-Akinese. Wien Klin Wschr 1961;73:787-8. 35. Laitinen LV, Bergenheim AT, Hariz MI. Leksell’s posteroventral pallidotomy in the treatment of Parkinson’s disease. J Neurosurg 1992;76:53-61. 36. Vogel S. Mo¨glichkeiten und Grenzen der Neurotransplantation. In: Poewe W, Madeja DU, editors. Aktuelle Aspekte der Therapie des Parkinson-Syndroms. Karlsruhe: Braun; 1991. p. 73-81. 37. Krauss JK, Volkmann J: Tiefe Hirnstimulation. Darmstadt: Steinkopff; 2004.

8 History of Stereotactic Surgery in Great Britain E. A. C. Pereira . A. L. Green . D. Nandi . T. Z. Aziz

The Horsley–Clarke Apparatus Stereotaxis was the name given to a procedure and apparatus invented in London by the Englishmen, Horsley and Clarke. Before then, the German Dittmar had used a guided probe to transect rodent medulla in 1873 [1], and Zernov in Russia had described an encephalometer enabling brain surface localization in 1889 [2]. Neither technique enabled targeting with respect to a fixed threedimensional Cartesian coordinate system. Sir Victor Alexander Haden Horsley (1857–1916; > Figure 8-1a) was the first neurophysiologist who was also a neurosurgeon, pioneering a Great British tradition of such hybrid scholars particularly prevalent in the stereotactic comamunity. His uniquely deft approach to neurosurgery – derived from experiments upon over 100 primates – made a reputation such that ‘‘the Staff intended to have Horsley and nobody else’’ when tenure became available at the National Hospital for the Paralyzed and Epileptic in Queen Square in 1886 [3,4]. Robert Henry Clarke (1850–1926; > Figure 8-1b) studied medicine at St. George’s Hospital in London before surgical training in Glasgow. He worked with Horsley in London in the late 1880s [5]. Throughout the following decades, they became intellectually consumed by the experimental challenges of cerebral localization of motor function following the seminal work of Hughlings Jackson and others. Clarke traveled to Egypt in the early 1890s to convalesce after developing aspiration pneumonia from aspirin inhalation. While there, gazing up at the stars, he conceived an apparatus through #

Springer-Verlag Berlin/Heidelberg 2009

which probing intracranial instruments could be inserted that could be clamped to an animal’s head fixing it to a Cartesian co-ordinate system by skull pins placed laterally, bars attached to plugs inserted into the external auditory meatus and further bars resting upon the nose and orbital margins. The idea was presented to Horsley on return to England [6]. A decade later in 1905 James Swift, a machinist at Palmer & Company in London, was commissioned to construct the first machine from brass, ‘‘Clarke’s stereoscopic instrument employed for excitation and electrolysis,’’ comprising frame, carrier and needle holder and costing £300 (> Figure 8-2) [7]. Results were published in 1906 from experimental use of the first instrument for targeting electrolytic lesions in the deep cerebellar nuclei of non-human primates [8]. In 1908 they described the apparatus and its use in greater depth, coining the term ‘‘stereotaxic’’ from the Greek ‘‘stereos’’ meaning ‘‘solid’’ and ‘‘taxis’’ meaning ‘‘arrangement,’’ commenting that ‘‘by this means every cubic millimeter of the brain could be studied and recorded’’ [9]. Although Clarke suggested that the apparatus might be useful in humans, neither he nor Horsley pursued the idea and shortly afterwards they ceased collaboration. Yet Clarke patented the apparatus including its proposed use in humans in 1914 and devoted much time to its improvement. By 1920, a rectilinear modification enabling needle inclination at different angles in an equatorial frame enabling 360 of movement were described (> Figure 8-2) [10]. Three others used the original apparatus in London for experimental work; first the visiting

78

8

History of stereotactic surgery in great britain

. Figure 8-1 (a) Sir Victor Alexander Haden Horsley; (b) Robert Henry Clarke (courtesy of the Wellcome Library, London)

American surgeon Ernest Sachs who studied the optic thalamus [11], then the neurologist S.A. Kinnier Wilson who studied the basal ganglia of 25 monkeys using the ‘‘Clarke-Horsley machine’’ [12]. Clarke’s original instrument was last utilized by Barrington, a London urologist who used it to study the effect of brain lesions upon micturition in cats [13]. Barrington died suddenly in 1956. Among the contents of his laboratory, ‘‘in true British fashion, was a biscuit tin’’ that contained parts of the original apparatus. After several inquiries, a technician in the Royal Veterinary College where Barrington had once worked produced a mahogany box containing the original model and it was returned to University College London in 1970. It now resides in the Science Museum in London, having been promoted from closed storage to prominent display by Tipu Aziz in 2000 (> Figure 8-3). Two further apparatus designs were made for Clarke by machinists Goodwin and Velacott also of Palmer & Company in London and exported to the United States for animal research soon after the First World War, the latter to Johns Hopkins

after agreement that the Baltimore institution would publish Clarke’s stereotaxic atlas [14]. Another of Horsley’s students, Aubrey Mussen also contemplated translation of Horsley-Clarke stereotaxis to humans. Mussen purchased one of the original Horsley-Clarke apparatus secondhand for £100 while working at the National Hospital in London from 1905 to 1906 and returned to McGill University with it, subsequently publishing results from studies of the hypoglossal nuclei that Horsley traversed with his deep cerebellar lesions [15]. Mussen designed further stereotactic instruments with Clarke, including a ‘‘cyclotome,’’ a probe used to make disk-shaped incisions along its axis and a ‘‘spherotome’’ used to cut spherical volumes bearing much resemblance to Anto´nio Egas Moniz’ leucotome [10]. Mussen designed and had commissioned a modification of the Horsley-Clarke apparatus for use in humans in 1914 on his return to London. It was completed around 1918, again in brass, and most likely again by Palmer & Company (> Figure 8-4). In the frame, electrode holders slid along horizontal graduated bars or vertical corner

History of stereotactic surgery in great britain

8

. Figure 8-2 Clarke and Horsley’s 1905 primate stereotaxic apparatus, showing also Clarke’s 1920 equatorial modification (top left), (courtesy of the Wellcome Library, London)

posts enabling orthogonal approaches to intracranial structures in anteroposterior and lateral directions. The apparatus required a human brain atlas and Mussen envisaged its use to thermocoagulate tumors using ‘‘Galvanic current. . .through a 5 mm trephine in the skull and puncturing the dura without exposing the brain at all’’ [17]. In the two decades that followed, Mussen neither completed the human atlas nor convinced neurosurgical colleagues to take up use of his frame [18]. He wrapped the unused British made apparatus in newspaper dating from the 1940s and placed it in his loft [19].

After Horsley’s original experiments, Sachs, Wilson and Barrington all had loan of the original Horsley-Clarke frame. Sachs and Mussen utilized Clarke’s second and third frames respectively for animal experiments in North America throughout the 1920s [20,21], as did others during the following decade. However, at least two key challenges remained in translating experimental animal stereotaxis into a clinical tool. Firstly there was great variability between human skull landmarks and cerebral structures and secondly humans could not be sacrificed as animals were to enable confirmatory histology of accurate targeting - and thus experimental validity. Three decades on from

79

80

8

History of stereotactic surgery in great britain

. Figure 8-3 The senior author with one of the original HorsleyClarke frames in 2000

major advances were firstly to create a frame tailored to the individual skull by means of a plaster skull cap and secondly to align their so-called ‘‘stereoencephalatome’’ not just to skull but to brain landmarks like the calcified pineal gland and foramen of Monro by means of intraoperative pneumoencephalography.

Post-War Innovation

. Figure 8-4 Mussen’s circa 1918 human stereotactic instrument (after Picard et al. [16])

Horsley and Clarke’s work, Spiegel and Wycis devised an apparatus for stereotactic neurosurgery in humans, publishing their achievement in 1947 [22]. The North Americans established ‘‘stereotactic’’ as the preferred term, fusing Greek with the Latin word ‘‘tactis,’’ the pluperfect passive form of the verb ‘‘tangere’’ meaning ‘‘to touch.’’ Their

With two World Wars, British stereotactic surgery remained fallow for the half century after Horsley’s discovery, the discipline only reaching the clinic once word had spread of Spiegel and Wycis’ invention. At first, primary applications were for treating psychiatric disorders and later clinical usage diffused to movement disorders in the 1950s and chronic pain soon after. Ahead of the rest, an English crusader and two Scottish pioneers emerged, each a clinical polymath but with an academic focus. In London, Geoffrey Knight developed stereotactic subcaudate tractotomy for psychiatric disorders, treating hundreds of patients while his eminent contemporary Sir Wylie McKissock continued freehand approaches. In Edinburgh, John Gillingham established stereotactic surgery for multiple clinical indications, designing his own stereotactic frame. In turn, his talented associate Ted Hitchcock was inspired first at Edinburgh and then in Birmingham to pioneer stereotactic approaches to the high cervical spinal cord and brainstem. Francis John Gillingham (b.1916; > Figure 8-5) trained in St. Bartholomew’s Hospital in London before entering the neurosurgical faculty at Edinburgh in 1950. Gillingham spent 12 years as first assistant to Norman McOmish Dott, one of the great triumvirate alongside Sir Hugh Cairns in Oxford and Sir Geoffrey Jefferson in Manchester, the Cushing apostles who definitively established neurosurgery as a specialty in Great Britain [24–26]. Gillingham was a brilliant and pioneering aneurysm surgeon

History of stereotactic surgery in great britain

8

. Figure 8-5 Francis John Gillingham (left) preparing for a stereotactic thalamotomy in 1968 (after Housepian 2004 [23])

like his mentor Dott [27,28]. A passionate educator, he also introduced the concept of subspecialty fellowships to British neurosurgical training [29], but stereotactic surgery received his greatest contributions. The Parisian neurosurgeon Gerard Guiot. introduced Gillingham to stereotactic surgery. They had become friends after Guiot visited Edinburgh to learn aneurysmal surgery from Dott and Gillingham. Guiot’s 1953 telegram to Gillingham read ‘‘I have something interesting to show you – come over.’’ Four days were spent performing freehand pallidotomies to treat parkinsonism under local anesthesia using a subfrontal approach to the anterior perforated substance interrupting the ansa lenticularis as described by Fenelon and Thiebaut following the seminal discoveries of Cooper [30–32]. Gillingham returned to Edinburgh to treat two patients in 1955 and 1957, reporting improvements in tremor, rigidity and quality of life. Wishing to reduce risks from the demanding subfrontal approach, he adapted Guiot’s stereotactic method [33]. In 1960 he published results from stereotactic ‘‘thermal electrocoagulation lesions of the globus pallidus, internal

capsule and thalamus either separately or in combination’’ in a further 58 patients operated upon from 1957 to 1959 [34]. In addition to globus pallidus and internal capsule, he began targeting the ventrolateral thalamus for refractory tremor based on work by Hassler [35]. ‘‘Of these (60) patients 53, or 88%, had tremor and/or rigidity abolished or significantly reduced without complications’’ [34]. From his early clinical results, Gillingham drew several conclusions. On targeting he wrote that ‘‘The best type of lesion. . .would seem to be the double one, made at the same time in the ventro-lateral nucleus of the thalamus and in the globus pallidus 16mm from the mid-line, both lesions bordering on the internal capsule. . .. Bilateral lesions in the treatment of bilateral Parkinsonism, provided they are small and strategically placed, would seem to be eminently practicable. . . usually with an interval of 3–6 months between the two operations.’’ On his modification of Guiot’s stereotactic apparatus he felt ‘‘that the merits of this method lie in the relatively short operative procedure and in its accuracy and simplicity. Its principles are based

81

82

8

History of stereotactic surgery in great britain

on the fact that the globus pallidus and thalamus bear a reasonably constant anatomical relationship to the anterior and posterior commissures, the intercommissural line, and the mid-sagittal plane of the head. . .. The method used has evolved progressively, and is unique, in allowing the creation of lesions in the globus pallidus, internal capsule, or thalamus with one electrode track at different depths’’ [34]. In their stereotactic apparatus design, Guiot and Gillingham favored operative principles to prioritize patient comfort, not restricting their movements by clamping their head, and to reduce laborious calculations. Guiot planned a parasagittal approach using intraoperative encephalography to delineate the midline and intercommissural point. Gillingham favored an occipitoparietal entry to avoid striate arteries and horizontal patient positioning to reduce putative brain shift. Thus the Guiot-Gillingham stereotactic apparatus was devised (> Figure 8-6). Radioopaque midline markers were used for the procedure and a 1 mm steel ball placed in each 5 mm lesion for subsequent charting. Over the . Figure 8-6 The Guiot-Gillingham stereotactic apparatus using a posterior rather than a coronal approach (after Gillingham et al. [34])

post-operative weeks, the ball was seen to fall through the necrotic lesion on skull radiographs, elegantly providing an estimate of lesion size. The frame’s conception preceded Hassler’s targeting of the thalamus for tremor and hence Gillingham attributed to serendipity that his posterior approach enabled multiple targets to be lesioned in a single pass [36]. Despite impressive clinical outcomes, Gillingham noted some inaccuracy to his lesions in the context of Brierley and Beck’s demonstration that relationships between basal ganglia structures and commissural landmarks were highly variable [37,38]. David Whitteridge, his neurophysiologist colleague at Edinburgh, had demonstrated to him in 1961 how microelectrode recording could distinguish between grey and white matter and thus delineate the lateral geniculate nuclei in the cat [39]. He immediately saw its utility for distinguishing functionally between deep brain structures and, with his colleague Michael Gaze, developed the technique for humans as did Guiot [40]. Fundamental physiological insights were gained in the quest to improve lesion accuracy and clinical efficacy, including spontaneous rhythmical discharge in the thalamus found to be synchronous with tremor [41]. Using microelectrode recording, target localization could be done accurately with a margin of error less than 1mm. Gillingham evolved the Guiot-Gillingham apparatus throughout the 1960s and 1970s, He added a phantom to allow an oblique track to more medial brain targets for epilepsy and psychiatric disorders, then an inferior extension to the posterior limb of the frame for targeting the cerebellum, brain stem and cervical spine in chronic pain and dystonias [42]. In 1977 he added a motor to automatically drive an electrode in at a slow and measured rate for microelectrode recording. Stereotactic surgery for deep hematomas and tumor biopsies was also performed [43]. Ten year follow-up in the post levodopa era of a second 60 patient parkinsonian cohort of Gillingham’s operated upon between

History of stereotactic surgery in great britain

1965 and 1967 showed decline in efficacy for bradykinesia, but consistent relief of tremor and rigidity [44]. Gillingham remained engaged in academic neurosurgery well into his ninth decade [45]. As Gillingham was Dott’s prote´ge´, so Ted Hitchcock was Gillingham’s. Edward Robert Hitchcock (1929–1993) studied medicine at Birmingham then neurosurgery at Oxford before joining the Edinburgh staff at the then recently opened Western General Hospital in 1965. While there, he received unique exposure to Gillingham’s stereotactic surgery which attracted international renown [23]. Hitchcock’s developed an interest in chronic pain and in particular the concept of percutaneous high spinal stereotactic commissural myelotomy. This procedure aimed to divide the decussating spinothalamic tracts through a targeted lesion and reduce the risks of respiratory paralysis conferred by open cordotomy. It was aimed at chronic cancer pain. It required access below the plane of a versatile frame, thus he invented his own target-centered arc system secured on a hollow square aluminum base ring secured to the skull by three-point fixation (> Figure 8-7). Vertical and horizontal bars determined probe length and laterality. The system was first used both for surgery and for microelectrode recording in the spinal cord by

. Figure 8-7 Hitchock’s stereotactic apparatus for brainstem and cervical spine surgery (after Hitchcock [46])

8

percutaneous approach using portable radiographs [46–48]. Hitchcock reported initial results of good or complete pain relief in 13 out of 19 patients at follow-up ranging from 1 week to 4 years [49]. A stereotactic pontine approach to spinothalamic tractotomy and to the trigeminal nucleus for anesthesia dolorosa was also applied [50–54], as were approaches to the thalamus and dentate nucleus to treat dystonia and in particular the spasticity of cerebral palsy [55]. The rationale behind the stereotactic pontine spinothalamic approach was to provide good analgesia with minimal risks to respiration, micturition and upward gaze [54]. Hitchcock wrote of his apparatus in the early 1970s that ‘‘the design and construction make this one of the most accurate, adaptable and simplest of modern stereotactic instruments’’[56]. Hitchcock became Professor of Neurosurgery at Birmingham in 1978, succeeding Brodie Hughes (1913–1989) who was also an established stereotactic surgeon [57,58]. Hitchcock put his stereotactic frame to many further clinical uses including biopsy of supratentorial, infratentorial and high spinal tumors and intraventricular masses [59–61], foreign body removal [62], realtimeclippingofotherwiseinoperablearteriovenous malformations [56], image-guided craniotomies [63], and in the 1980s in the planning and treatmentstagesofradiosurgery[64].Thesemanyvaried clinical indications in brain and spine earned him the nickname ‘‘Columbus of the brain’’ in the local clinical neuroscience community. At the MidlandHospitalforNeurologyandNeurosurgery, he used his stereotactic expertise to established a programme at first for adrenal medullary and then in the late 1980s for fetal mesencephalic transplantation in Parkinson’s disease, performing the procedure on 55 patients [65–68]. Neurosurgery for psychiatric disorders in Great Britain echoed its popularization in the United States following Freeman and Watts’ simplification of Moniz’ procedure in the 1940s [69,70]. Its foremost British proponent was the

83

84

8

History of stereotactic surgery in great britain

London neurosurgeon Sir Wylie McKissock (1906–1994), founder of the neurosurgical department at Atkinson Morley’s Hospital in Wimbledon [71]. McKissock favored a freehand approach to the frontal lobe from above [72]. He described the rostral leucotomy in 1951 as a rejoinder to Freeman and Watt’s transorbital ‘‘icepick’’ leucotomy which he considered to contravene ‘‘established aseptic surgical principles’’ [73,74]. McKissock’s immense South England practice and his reputation for extraordinary surgical speed inculcated a peripatetic service visiting other hospitals in his car with his surgical instrument set in the boot, drawing parallels with Freeman [75,76]. It is suggested that McKissock alone may have performed one quarter of the 10,365 procedures performed in the United Kingdom from 1942 to 1954 [77]. Geoffrey Cureton Knight (1906–1994) of Hammersmith and Brook Hospitals in London and Woolwich saw more readily than McKissock the merits of stereotactic over freehand approaches in reducing the morbidity and mortality of neurosurgery for psychiatric disorders [74,78]. After his freehand experience [79], Knight created the procedure of stereotactic subcaudate tractotomy in 1961 using a modified stereotactic device that his London colleague the Scottish neurosurgeon Ian Reay McCaul (1916–1989) reported in 1959 [58,80]. His first few hundred orbital undercuttings led him to conclude that lesions extending posteriorly under the caudate were most efficacious and that the last 2 cm was key [81,82]. Knight used bony landmarks on lateral radiographs, and later air encephalography to guide him. In addition, he employed brachytherapy as an ablative tool, implanting radioactive Yttrium (Y90) to create flat lesion approximately 20 by 20 by 7 mm (> Figure 8-8) [83–85]. The treatment proved effective and endured four decades amid decline in use of other psychosurgical treatments. The group described treatment of 1,300 patients with ‘‘non-schizophrenic affective disorders,’’ 40–60% going on to live normal or near normal lives with a reduction in

. Figure 8-8 Anteroposterior radiograph of Geoffrey Knight’s stereotactic subcaudate tractotomy showing yttrium seeds in situ for brachytherapy (after Knight [83])

suicide rates from 15 to 1% [86,87]. Long-term outcomes were published by the psychiatrist Bridges and the London neurosurgeon John Bartlett, Knight’s successor from 1972. Following the retirement of Knight, the unit was named the Geoffrey Knight Unit for Affective Disorders to emphasize Knight’s appreciation of the fundamental importance of psychiatric evaluation both in diagnosis and in full consideration of medical treatments prior to offering surgery. In 1996 the unit moved to the Maudsley Hospital and Y90 production ceased. Bartlett adapted a Leksell frame arc compatible with modern neuroimaging using concepts that underlay the McCaul device. Radiofrequency lesioning replaced radioisotope implantation [88,89]. It is a tribute to Knight that McKissock’s colleague at Atkinson Morley’s Hospital, Alan Richardson (1926–1998), adopted a stereotactic approach for his psychiatric procedures [72]. Together with his psychiatrist colleague Desmond Kelly, he combined Knight’s subcaudate tractotomy with a cingulotomy to invent the procedure of limbic leucotomy in the early

History of stereotactic surgery in great britain

1970s [90,91]. It is interesting to note that cingulectomy for psychiatric disorders was first performed in 1948 in Oxford by Sir Hugh Cairns, albeit freehand [92]. Both Knight’s subcaudate tractotomy and Richardson’s limbic leucotomy continue to be performed in carefully selected cases refractory to medical treatment worldwide including in Great Britain and elswehere [93–95]. Stereotactic neurosurgery was embraced by Dott’s unit in Edinburgh and, at Oxford after Cairns, Pennybacker appointed Watkins to establish a service, but other regions were also keen to commence it. In Manchester, Jefferson’s successor Richard Johnson appointed John Dutton to undertake a high volume of ablations for parkinsonism and other stereotactic procedures throughout the 1960s using a Leksell frame. Soon after, John Gleave (1925–2006) established a stereotactic service in Cambridge also using a Leksell frame, treating parkinsonism with cryosurgery and developing a side-cutting stereotactic biopsy cannula [96,97]. Other British neurosurgeons like McCaul made and modified stereotactic frames. Of particular note was the frame of Alfred Michael Bennett (1920–1996) and his use of a sphere inserted into a burr hole to aid targeting [98,99]. Bennett’s apparatus were popular locally, used by Sid Watkins and later David Thomas in London amongst others [100,101]. Most designs were less radical and therefore perhaps less memorable than those of Gillingham and Hitchcock.

Stereotactic Atlases Horsley and Clarke produced the first stereotaxic atlas, a monkey version appearing in their 1908 publication. Later publications were by Clarke at first for the cat in collaboration with the British ophthalmic surgeon E. Erskine Henderson in 1912 and later by Clarke alone for the monkey in 1920 [10,102,103]. Both atlases comprised brain slices 2 mm thick. The latter atlas showed sections of monkey brain at calibrated intervals

8

with a scale giving slice thickness and height from the base of the apparatus. Sections were registered by a Cartesian coordinate system to the skull landmarks of inferior orbital rim and both external auditory canals to which the frame was fixed. Zero axes were the plane between these structures axially, the mid-sagittal plane and the coronal plane between both external auditory meatus orthogonal to both other planes. The human brain atlases produced outside Great Britain, in particular by Spiegel and Wycis, Schaltenbrand and Bailey and Talairach transformed stereotactic functional neurosurgery. Schaltenbrand detailed anatomical nuclei with an emphasis on the thalamus and adjacent deep brain structures now used in deep brain stimulation for movement disorders and Talairach revealed vasculature relevant to epilepsy surgery [104–106]. The British neurosurgeon Sid Watkins also made rigorous contributions. Eric Sidney Watkins (b.1932) was given the task of starting stereotactic neurosurgery at the Radcliffe Infirmary in Oxford in the 1950s by Joe Pennybacker. Dissatisfied with the variability of basal ganglia structures with respect to the frequently uncalcified and thus radiolucent pineal gland using the Spiegel and Wycis atlases, he used the Schaltenbrand and Talairach atlases that appeared shortly after. Initially globus pallidus and ansa lenticularis were targeted for Parkinsonian rigidity, tremor and dystonia then later the lateral thalamus in the 1960s. The desire to create his own atlas arose in the early 1960s from a wish to commence thalamotomy for pain and a concern at the adequacy of available atlases to accurately enable targeting based upon anatomy alone in the absence of subjective or physiological guidance. Encouragement came from London neurosurgical colleagues John Andrew and Valentine Logue who were also keen to begin such therapies. Another atlas that became available was created by Brierley and Beck who sectioned 40 brains in 3–5 mm slices, relating them in a proportional hypothesis for thalamic nuclear determination to

85

86

8

History of stereotactic surgery in great britain

anterior and posterior thalamic limits and the midthalamic point and describing great individual variations [38]. Watkins found the atlas to be limited clinically as the use of simultaneous positive and air ventriculography using air in the ambient cisterns to outline the pulvinar nuclei and thus the thalamic limits was not consistently reproducible. In the 1960s at the National Hospital for Nervous and Mental Diseases together with Watkins then at the Royal London Hospital, John Andrew produced a greatly enlarged atlas with drawings defining in detail deep brain nuclei including the thalamus and its relations [107]. The atlas was based upon 38 formalin fixed brains. It measured the position of the thalamic centromedian nucleus using 1 mm coronal slices with reference planes between the posteroinferior margin of the foramen of Monro and posterior commissure and the midpoint between the ventricular surfaces of the anterior and posterior commissures. Its utility lies in the presentation of statistical data in a graphic form together with stereotactic coordinates superimposed on simple line drawings of the thalamus. In 1978 at the London Hospital, Fari Afshar detailed brain stem and cerebellar nuclei, again under Sid Watkins’ supervision [108]. The impetus for the Afshar atlas came from an interest in attempting to ameliorate spasticity in cerebral palsy by ablation of the cerebellar dentate nucleus. Approximately 30 brains were prepared using positive-contrast ventriculography with skull and brain mounted in a stereotactic frame in order to accurately correlate structures with coordinates. Again, formalin fixation of 1mm slices was performed. Modified Mulligan stain was used and each section magnified, with drawings made using a camera lucida. Reference plains were the fourth ventricular floor and fastigium and the midsagittal plane. As before, variability profiles were quantified and standard deviations presented. Both Watkins atlases are resources used today to help ratify localization and indeed the

Afshar atlas continues to augment heated debates regarding the targeting of the novel functional neurosurgical treatment of deep brain stimulation of the pedunculopontine region for Parkinson’s disease [109,110]. Watkins has commented upon the major difficulties in measurement due to distortion related to fixation and shrinkage, past atlases suffering from approximately 10% shrinkage. To reduce shrinkage to 2–5%, he utilized Corsellis’ technique – a ten day formalin suspension after removing brain and skull en bloc minus the frontal and facial bones [111]. To appease undertakers’ concern at cosmetic consequences, each cadaver’s scalp was replaced over a plaster of Paris prosthesis fixed to a broom handle on a nail inserted into the cervical canal. However, cremation of the augmented cadavers became suboptimal, precipitating a strike among undertakers serving the London Hospital by the time Afshar’s posterior fossa atlas had reached its completion [112].

Computed Tomography By the late 1970s, British stereotactic functional surgery was a decade on from its first successes, having declined with the advent of neuropsychopharmacology. Levodopa was introduced to relieve Parkinson’s disease [113], chlorpromazine and monoamine oxidase inhibitors to ameliorate schizophrenia and depression respectively, and the case series showing good relief after lesional surgery for chronic pain paled against a background of new analgesics and peripheral neuromodulatory therapies. Stereotactic approaches to tumors had been established but most neurosurgeons did not train in stereotactic neurosurgery. Hitchcock continued psychiatric procedures for medically refractory depression, obsessivecompulsive disorders and anxiety alongside Bartlett and Richardson, but the developing subspecialty sought advances in other domains. Enter the British engineer.

History of stereotactic surgery in great britain

Sir Godfrey Newbold Hounsfield (1919– 2004; > Figure 8-9) joined EMI in Hayes, Middlesex in 1951, having been first a mechanic first of radios then later radars in the Royal Air Force and obtained a diploma from Faraday House Electrical Engineering College in London. At EMI he worked first on radars and guided weapons, then the first all-transistor computers. During a weekend ramble in 1967 he conceived what later became the first EMI-scanner and the technique of computed tomography (CT), which he recounted as ‘‘a realization that you could determine what was in a box by taking readings at all angles through it.’’ Recording multiple pictures from a rotating X-ray source, a series of slices could be photographed and a three-dimensional image reconstructed from the slices. After initial successful experiments with a cylindrical phantom containing radio-opaque objects in his Hayes laboratory using X-rays, Hounsfield forged a collaboration . Figure 8-9 Sir Godfrey Hounsfield at the controls of the EMI scanner in Atkinson Morley’s Hospital in London (after Petrik et al. [114])

8

with James Ambrose, radiologist at Atkinson Morley’s Hospital, to translate the device’s utility to humans. McKissock gave the endeavor his blessing [75]. Hounsfield set to work on bullock’s heads obtained from a kosher slaughterhouse in East London to obviate the traumatic intracranial hemorrhage seen after conventional slaughter [114]. Ambrose interpreted the early scans and suggested the use of sodium iothalamate contrast to highlight tumors [115]. His early interpretations and predictions formed the basis of contemporary diagnostic neuroradiology [116,117]. The first patient was scanned in 1971, revealing a cyst [118]. In 1979 Hounsfield was awarded the Nobel Prize for Physiology or Medicine together with Allan Cormack, the Cape Town physicist whose mathematical theories Hounsfield had realized [119]. The advent of CT breathed new life into stereotactic surgery in Britain. Several neurosurgeons began to experiment with CT compatible apparatus, both imported, usually Leksell, and those of Gillingham and Hitchcock [36,120]. Magnetic resonance imaging (MRI) followed shortly after, again with frames being modified as required. After a quiescent decade, the late 1980s augured for a renaissance. Alongside emerging limitations of drug therapies for movement disorders resurrecting clinical indications for functional neurosurgery, great advances came from increasing computer power enabling the fusion of more spatially robust CT information with the greater soft tissue detail of MRI and comparison to computerized brain atlas images. In Britain, the current generation of senior stereotactic neurosurgeons were gaining their clinical training and conducting their first research, some in classical stereotactic methods abroad, some by subspecialty fellowships in Britain thanks to Gillingham’s enduring influence upon neurosurgical programmes, and others by animal experiments true to Horsley’s hybrid scientist-surgeon mould. The stage was set for two decades of rapid advances in British stereotactic neurosurgery.

87

88

8

History of stereotactic surgery in great britain

Radiosurgery Lars Leksell’s brilliance showed not only in his frame design [121], employing the novel arcquadrant principle, but also in his insight that focused radiation could be used as the tool. Many intersecting radiation beams focused towards a target would result in a high cumulative radiation dose, with radiation intensity declining rapidly with distance from the ‘‘isocenter.’’ Thus, a deep brain structure could be lesioned noninvasively by focused radiation. The technology of ‘‘radiosurgery’’ could be applied to acoustic neuromas, arteriovenous malformations and other discrete pathologies [122]. Britain acquired one of the first gamma knives in 1985 at the same time as Argentina just 3 years on from the Falklands War. David Forster achieved incredible feats in leading the campaign to fund the device on the British National Health Service, building the infrastructure over 2 years to host it and ultimately purchasing the first custom-made unit in 1985. The National Centre for Stereotactic Radiosurgery was refurbished in 1991 and its cobalt sources renewed. The unit receives approximately one half to two thirds of all radiosurgery referrals from all over the United Kingdom. Approximately 500 cases a year are performed, a third of cases treated being ateriovenous malformations, with small to medium sized acoustic neuroma treatment having increased from 10% to one third over the period 1994–2001 and approximately 100 meningiomas and other skull base or recurrent tumors treated per year. Other indications treated have included trigeminal neuralgia, pituitary tumors and metastases, although the latter two indications are treated in smaller proportions than outside the United Kingdom, reflecting more conservative referral patterns [123]. For similar reasons, few epilepsy and functional cases have been performed. Several neurosurgical centers use linear accelerators to perform radiosurgery, each performing up to 40 cases per year. A gamma knife was also

acquired by the Cromwell Hospital in London in 1998, run privately by Christer Lindquist. It has treated 1,000 patients since installation and has recently been refurbished.

Functional Surgery European factors driving British stereotactic surgery included Benabid’s application of thalamic deep brain stimulation to Parkinson’s disease in 1987 and Laitinen’s reapplication of Leksell’s pallidotomy in 1992 [124,125]. Functional neurosurgery was resurrected at the Radcliffe Infirmary in Oxford four decades after Watkins’ departure under the headship of Mr. Christopher Adams [126]. We had already established with Alan Crossman in Manchester by the early 1990s at the same time as DeLong’s team across the Atlantic that lesions made to the subthalamic nucleus in primates reversed the motor symptoms of 1-methyl-4-phenyl-1,2,3,6tetrahydropyridine (MPTP) induced parkinsonism [127–129], At Oxford and Charing Cross Hospital in London, we undertook stereotactic surgery of this target and others [130–135]. At the same time we continued non-human primate research into establishing the pedunculopontine nucleus as a potential target for gait freezing and postural instability [136–139]. The former target is now the target of choice for Parkinson’s disease surgery and initial clinical results of the latter show great promise [140–143]. Other translational research at the University of Oxford and Imperial College London included invasive deep brain electrophysiological insights into tremor and dystonia [144–146], use of single photon emission tomography (SPET) [147], magnetoencephalography (MEG) [148], and diffusion tensor imaging (DTI)[149,150] to study deep brain stimulation and research into deep brain stimulation for pain and blood pressure control and brainstem control of exercise [151,152]. We have used deep brain stimulation to treat 70 patients

History of stereotactic surgery in great britain

with dystonia [153], 60 with chronic pain [154], and we perform one fifth of Britain’s movement disorders surgery. In Bristol, Professor Steven Gill has continued the Great British tradition of innovation, creating a stereotactic frame convenient for radiosurgery under Professor David Thomas’ supervision in London [155,156], and performing several clinical firsts including glial-cell derived neurotrophic factor infusion and pedunculopontine nucleus stimulation for Parkinson’s disease [157–160]. With Mr. Nikunj Patel, he continues to drive the field forward. After the retirement last decade of Mr. John Miles in Liverpool whose tremendous pain practice still left time for several innovations [161– 163], Professor David Thomas also recently

8

retired as the Gough-Cooper Professor of Neurosurgery at the National Hospital of Neurology and Neurosurgery at Queen Square. He had devoted three decades to the improvement of stereotactic surgical techniques with and without frames [164–168]. Britain welcomed Professor Marwan Hariz at Queen Square as the first Edmond J. Safra Chair of Functional Neurosurgery, ‘‘solving’’ the functional neurosurgery service there [169], and establishing a biennial international workshop like its host, unsurpassed for its conviviality and candour (> Figure 8-10). Almost all of the 34 hospitals conducting neurosurgery in Great Britain and Northern Ireland have consultants able to offer stereotactic surgery a century on from Horsley’s first experiments. A third of these hospitals have

. Figure 8-10 The faculty of the International Workshop on Functional Neurosurgery for Movement Disorders and Mental Illness & Commemoration of the 150th Anniversary of the Birth of Sir Victor Horsley, London, 2007 (courtesy of Professor Marwan Hariz). Back Row from left to Right: Lazaro Alvarez La Habana, Peter Brown, Gun Marie Hariz, Paul Krack, Pierre Pollak, Bart Nuttin, Roger Melvill, Steven Gill, Patricia Limousin-Dowsey, Niall Quinn, John Rothwell, Veerle Visser-Vandewalle, Roger Lemon, Rees Cosgrove, Andres Lozano, Laura Cif, Ludvic Zrinzo, Marjan Jahanshahi, Stephen Tisch, Hans Speelman, Philippe Coubes, Pat Forsdick. Front Row Left to Right: Takaomi Taira, Jean-Luc Houeto, Alim-Louis Benabid, Tipu Aziz, Boulos-Paul Bejjani Byblos, Alan Crockard, Marwan Hariz, Carmelo Sturiale

89

90

8

History of stereotactic surgery in great britain

subspecialty trained stereotactic surgeons offering functional procedures, the majority of them affiliated to universities and conducting clinical or translational research. Far from being the reserve of the eccentric scientist-surgeons looked upon with suspicion by the rest of the neurosurgical fraternity, stereotactic surgery has become an established clinical subspecialty and academic discipline in its own right. The Society of British Neurological Surgeons formed in 1929 has recently begun devoting specific sections to stereotactic and functional neurosurgery at its meetings. A further society with a focus upon pain that welcomes stereotactic neurosurgeons, the Neuromodulation Society of the United Kingdom and Ireland (NSUKI) was founded in 2001. Such factors prove good indicators of the definitive establishment of the subspecialty in the United Kingdom. Phil Gildenberg has commented that there are four central tenets of the field of stereotactic surgery [170]. The need to be innovative – that a better way to do something may be more apparent to the most junior member of the team rather than the most senior. That stereotactic surgeons work as a community not in isolation. That stereotactic surgery is, to a large extent, a basic science. Although not appealing to the neurosurgeon interested only in a better way to cut, it is exciting to one appreciating the associated basic science. Finally, there is awed appreciation for the insight and courage of the true pioneers in the field. The British school exemplifies such values. It is hoped that its practitioners will continue to uphold tradition as we look to the future with excitement.

Acknowledgments We thank Mr. John Bartlett for helpful comments, Professor David G. T. Thomas, Professor Anthony J. Strong, Professor John D. Pickard, Mr. Robert Macfarlane and Mr. Colin Watts for advice on historical sources and Professor Marwan I. Hariz

for helpful comments and advice on > Figure 8-10. The authors receive financial support for research from the UK Medical Research Council, Normal Collisson Foundation, Charles Wolfson Charitable Trust and Oxford Partnership Comprehensive Biomedical Research Centre.

References 1. Dittmar C. Ueber die Lage des sogenannten Gefaesszentrums in der Medulla oblongata. Bersaechs Ges Wiss Leipzig (Math Phys) 1873;25:449-69. 2. Zernov DN. Encephalometer: device for estimation of parts of brain in human. Proc Soc Physicomed Moscow Univ 1889;2:70-80. 3. Paget S. Sir Victor Horsley: a study of his life and work. New York: Harcourt, Brace and Howe; 1920. 4. Northfield WC. Sir Victor Horsley, his contributions to neurological surgery. Surg Neurol 1973;1:131-4. 5. Davis RA. Victorian physician-scholar and pioneer physiologist (Robert Henry Clarke). Surg Gynecol Obstet 1964;119:1333-40. 6. Sachs E. Victor Horsley. J Neurosurg 1958;15:240-4. 7. Schurr PH, Merrington WR. The Horsley-Clarke stereotaxic apparatus. Br J Surg 1978;65:33-6. 8. Clarke RH, Horsley V. On a method of investigating the deep ganglia and tracts of the central nervous system (cerebellum). Br Med J 1906;2:1799-800. 9. Horsley V, Clarke RH. The structure and functions of the cerebellum examined by a new method. Brain 1908;31:45-124. 10. Clarke RH. Part I: Investigation of the central nervous system, methods and instruments. Baltimore, MD: Johns Hopkins; 1920. 11. Sachs E. On the structure and functional relations of the optic thalamus. Brain 1909;32:95-186. 12. Wilson SAK. An experimental research into the anatomy and physiology of the corpus striatum. Brain 1914;36:427-92. 13. Barrington FJF. The effect of lesions of the hind- and midbrain on micturition in the cat. Q J Exp Physiol 1925;15:81-102. 14. Fodstad H, Hariz M, Ljunggren B. History of Clarke’s stereotactic instrument. Stereotact Funct Neurosurg 1991;57:130-40. 15. Mussen AT. Notes on the movements of the tongue from stimulation of the twelfth nucleus, root and nerve. Brain 1909;32:206. 16. Picard C, Olivier A, Bertrand G. The first human stereotaxic apparatus. The contribution of Aubrey Mussen to the field of stereotaxis. J Neurosurg 1983;59:673-6. 17. Bertrand G. Stereotactic surgery at McGill: the early years. Neurosurgery 2004;54:1244-51; discussion 1251-2.

History of stereotactic surgery in great britain

18. Jensen RL, Stone JL, Hayne R. Use of the Horsley-Clarke stereotactic frame in humans. Stereotact Funct Neurosurg 1995;65:194-7. 19. Gildenberg PL. The history of stereotactic neurosurgery. Neurosurg Clin N Am 1990;1:765-80. 20. Sachs E, Fincher EF. Anatomical and physiological observations on lesions in the cerebellar nuclei in Macacus rhesus (preliminary report). Brain 1926;50:350-6. 21. Mussen AT. Experimental investigations on the cerebellum. Brain 1927;50:313-49. 22. Spiegel EA, Wycis HT, Marks M, Lee AJ. Stereotaxic apparatus for operations on human brain. Science 1947;106:349-50. 23. Housepian EM. Stereotactic surgery: the early years. Neurosurgery 2004;55:1210-4. 24. Fraenkel GJ. Hugh Cairns: first Nuffield professor of surgery, University of Oxford. Oxford: Oxford University Press; 1991. 25. Rush C, Shaw JF. With sharp compassion: Norman Dott Freeman surgeon of Edinburgh. Aberdeen: Aberdeen University Press; 1990. 26. Schurr PH, Royal Society of Medicine (Great Britain). So that was life: a biography of Sir Geoffrey Jefferson, Kt CBE FRS MS FRCS (1886–1961): master of the neurosciences and man of letters. London: Royal Society of Medicine Press; 1997. 27. Todd NV, Howie JE, Miller JD. Norman Dott’s contribution to aneurysm surgery. J Neurol Neurosurg Psychiatry 1990;53:455-8. 28. Gillingham J. Proceedings: twenty-five years’ experience with middle cerebral aneurysms. J Neurol Neurosurg Psychiatry 1975;38:405. 29. Gillingham FJ. Surgical training in the EEC – the training of a specialist. Acta Neurochir (Wien) 1982;61:17-24. 30. Cooper IS. Ligation of the anterior choroidal artery for involuntary movements: parkinsonism. Psychiatr Q 1953;27:317-9. 31. Fenelon F, Thiebaut F. Resultats du traitment neurochirugical du syndrome parkinsonien par intervention direct sur les voies etrapyramidales immediatement sous-striopallidales (anse lenticulaire). Rev Neurol (Paris) 1950;83:437-40. 32. Guiot G, Brion S. Traitement des mouvements anormaux par la coagulation pallidale; technique et resultats. Rev Neurol (Paris) 1953;89:578-80. 33. Guiot G. Le traitement des syndromes parkinsoniens par la destruction du pallidum interne. Neurochirurgia (Stuttg) 1958;1:94-8. 34. Gillingham FJ, Watson WS, Donaldson AA, Naughton JA. The surgical treatment of parkinsonism. Br Med J 1960;2:1395-402. 35. Hassler R, Riechert T. Indikationen und lokalisations: methode de gezeilten hirnoperationen. Nervenarzt 1954;25:441-7.

8

36. Gillingham J. The Guiot-Gillingham Apparatus. In: Gildenberg PL, Tasker RR, editors. Textbook of stereotactic and functional neurosurgery. New York: McGraw Hill; 1998. p. 139-44. 37. Gillingham J. Introduction to the scientific sessions. Accidents in stereotaxy – side-effects or bonus? Acta Neurochir (Wien) 1974;Suppl 21:5–12. 38. Brierley JB, Beck E. The significance in human stereotactic brain surgery of individual variation in the diencephalon and globus pallidus. J Neurol Neurosurg Psychiatry 1959;22:287-98. 39. Gillingham FJ. Neurosurgery. Br J Surg 1966;53:833-6. 40. Guiot G, Hardy J, Albe-Fessard D. Delimination precise des structures sous-corticales et identification de noyaux thalamiques chez l’homme par l’electrophysiologie stereotaxique. Neurochirurgia (Stuttg) 1962;5:1-18. 41. Gaze RM, Gillingham FJ, Kalyanaraman S, Porter RW, Donaldson AA, Donaldson IM. Microelectrode recordings from the human thalamus. Brain 1964;87:691-706. 42. Gillingham FJ, Campbell D. Surgical interruption of the conduction pathways for the control of intractable epilepsy. Acta Neurochir Suppl (Wien) 1980;30:67-74. 43. Kalyanaraman S, Gillingham FJ. Stereotaxic biopsy. J Neurosurg 1964;21:854-8. 44. Kelly PJ, Gillingham FJ. The long-term results of stereotaxic surgery and L-dopa therapy in patients with Parkinson’s disease. A 10-year follow-up study. J Neurosurg 1980;53:332-7. 45. Gillingham J. Forty-five years of stereotactic surgery for Parkinson’s disease: a review. Stereotact Funct Neurosurg 2000;74:95-8. 46. Hitchcock E, Lewin M. Stereotactic recording from the spinal cord of man. Br Med J 1969;4:44-5. 47. Hitchcock E. Stereotaxic spinal surgery. A preliminary report. J Neurosurg 1969;31:386-92. 48. Hitchcock E. An apparatus for stereotactic spinal surgery. Lancet 1969;1:705-6. 49. Hitchcock E. Stereotactic myelotomy. Proc R Soc Med 1974;67:771-2. 50. Hitchcock E. Stereotactic trigeminal tractotomy. Farmatsiia 1970;19:131-5. 51. Hitchcock E, Kim MC, Sotelo M. Further experience in stereotactic pontine tractotomy. Appl Neurophysiol 1985;48:242-6. 52. Hitchcock E, Teixeira MJ. Pontine stereotactic surgery and facial nociception. Neurol Res 1987;9:113-7. 53. Hitchcock E, Sotelo MG, Kim MC. Analgesic levels and technical method in stereotactic pontine spinothalamic tractotomy. Acta Neurochir (Wien) 1985;77:29-36. 54. Hitchcock ER. Stereotaxic pontine spinothalamic tractotomy. J Neurosurg 1973;39:746-52. 55. Gornall P, Hitchcock E, Kirkland IS. Stereotaxic neurosurgery in the management of cerebral palsy. Dev Med Child Neurol 1975;17:279-86.

91

92

8

History of stereotactic surgery in great britain

56. Shieff C. The Hitchcock apparatus. In: Gildenberg PL, Tasker RR, editors. Textbook of stereotactic and functional neurosurgery. New York: McGraw Hill; 1998. p. 101-4. 57. Hughes B. Involuntary movements following stereotactic operations for parkinsonism with special reference to Hemi-Chorea (Ballismus). J Neurol Neurosurg Psychiatry 1965;28:291-303. 58. Lyle I, Taylor S. Lives of the fellows of the Royal College of Surgeons of England: 1983–1990. London: Royal College of Surgeons of England; 1995. 59. Hitchcock ER, Issa AM, Sotelo MG. Stereotactic excision of deeply seated intracranial mass lesions. Br J Neurosurg 1989;3:313-20. 60. Hitchcock E, Kenny BG. Stereotaxy of third ventricular masses. Acta Neurochir Suppl (Wien) 1989;46:82-5. 61. Hitchcock E, Morris CS. Immunocytochemical techniques in stereotactic biopsy. Stereotact Funct Neurosurg 1989;53:21-8. 62. Hitchcock E, Cowie R. Stereotactic removal of intracranial foreign bodies: review and case report. Injury 1983;14:471-5. 63. Hitchcock E. Open stereotactic surgery. Acta Neurochir Suppl (Wien) 1991;52:9-12. 64. Hitchcock E, Kitchen G, Dalton E, Pope B. Stereotactic LINAC radiosurgery. Br J Neurosurg 1989;3:305-12. 65. Hitchcock E. Stereotactic neural transplantation. Stereotact Funct Neurosurg 1994;62:120-33. 66. Hitchcock ER, Kenny BG, Clough CG, Hughes RC, Henderson BT, Detta A. Stereotactic implantation of foetal mesencephalon (STIM): the UK experience. Prog Brain Res 1990;82:723-8. 67. Hitchcock ER, Clough CG, Hughes RC, Kenny BG. Transplantation in Parkinson’s disease: stereotactic implantation of adrenal medulla and foetal mesencephalon. Acta Neurochir Suppl (Wien) 1989;46:48-50. 68. Kudoh C, Detta A, Meyer C, Byrne P, Hitchcock E. Bilateral intracaudate cografting of fetal ventral mesencephalon and striatum in advanced Parkinson’s disease. Transplant Proc 1999;31:3397-402. 69. Freeman W, Watts JW. Psychosurgery in the treatment of mental disorders and intractable pain. 2nd ed. Springfield, IL: C. C. Thomas; 1950. 70. Moniz E. Tentatives Ope´ratoires dans le Traitement de Certaines Psychoses. Paris: Masson; 1936. 71. Richardson AE. Sir Wylie McKissock. Surg Neurol 1988;30:173-4. 72. Kitchen N. Neurosurgery for affective disorders at Atkinson Morley’s Hospital 1948–1994. Acta Neurochir Suppl 1995;64:64-8. 73. McKissock W. Rostral leucotomy. Lancet 1951;2:91-4. 74. McKissock W. Discussion on psychosurgery. Proc R Soc Med 1959;52:206-9. 75. Bell BA. Wylie McKissock – reminiscences of a commanding figure in British neurosurgery. Br J Neurosurg 1996;10:9-18.

76. El-Hai J. The lobotomist: a maverick medical genius and his tragic quest to rid the world of mental illness. Hoboken, NJ: Wiley; 2005. 77. Tooth J, Newton M. Leucotomy in England and Wales 1942–1954: report on public health and medical subjects no. 104. London: Her Majesty’s Stationery Office; 1961. 78. Knight GC. Discussion on psychosurgery. Proc R Soc Med 1959;52:209-10. 79. Knight GC, Tredgold RF. Orbital leucotomy; a review of 52 cases. Lancet 1955;268:981-6. 80. McCaul IR. Stereotaxic surgery and involuntary movement. Proc R Soc Med 1961;54:378-80. 81. Knight G. The orbital cortex as an objective in the surgical treatment of mental illness. The results of 450 cases of open operation and the development of the stereotactic approach. Br J Surg 1964;51:114-24. 82. Knight G. Stereotactic tractotomy in the surgical treatment of mental illness. J Neurol Neurosurg Psychiatry 1965;28:304-10. 83. Knight GC. Bi-frontal stereotactic tractotomy: an atraumatic operation of value in the treatment of intractable psychoneurosis. Br J Psychiatry 1969;115:257-66. 84. Knight G. Neurosurgical aspects of psychosurgery. Proc R Soc Med 1972;65:1099-104. 85. Knight G. Further observations from an experience of 660 cases of stereotactic tractotomy. Postgrad Med J 1973;49:845-54. 86. Bridges PK, Bartlett JR, Hale AS, Poynton AM, Malizia AL, Hodgkiss AD. Psychosurgery: stereotactic subcaudate tractomy. An indispensable treatment. Br J Psychiatry 1994;165:599-611; discussion 612-3. 87. Hodgkiss AD, Malizia AL, Bartlett JR, Bridges PK. Outcome after the psychosurgical operation of stereotactic subcaudate tractotomy, 1979–1991. J Neuropsychiatry Clin Neurosci 1995;7:230-4. 88. Malhi GS, Bartlett JR. A new lesion for the psychosurgical operation of stereotactic subcaudate tractotomy (SST). Br J Neurosurg 1998;12:335-9. 89. Malhi GS, Bartlett JR. Depression: a role for neurosurgery? Br J Neurosurg 2000;14:415-22; discussion 423. 90. Kelly D, Richardson A, Mitchell-Heggs N. Stereotactic limbic leucotomy: neurophysiological aspects and operative technique. Br J Psychiatry 1973;123:133-40. 91. Kelly D, Richardson A, Mitchell-Heggs N, Greenup J, Chen C, Hafner RJ. Stereotactic limbic leucotomy: a preliminary report on forty patients. Br J Psychiatry 1973;123:141-8. 92. Williams LM. Arousal dissociates amygdala and hippocampal fear responses: evidence from simultaneous fMRI and skin conductance recording. Neuroimage 2001;14:1070-9. 93. Christmas D, Matthews K, Eljamel MS. Neurosurgery for mental disorder. Br J Psychiatry 2004;185:173-4; author reply 174. 94. Feldman RP, Alterman RL, Goodrich JT. Contemporary psychosurgery and a look to the future. J Neurosurg 2001;95:944-56.

History of stereotactic surgery in great britain

95. Kopell BH, Machado AG, Rezai AR. Not your father’s lobotomy: psychiatric surgery revisited. Clin Neurosurg 2005;52:315-30. 96. Marks PV, Wild AM, Gleave JR. The ‘Cambridge’ stereotactic biopsy instrument. Br J Neurosurg 1990;4:127-8. 97. Wild AM, Xuereb JH, Marks PV, Gleave JR. Computerized tomographic stereotaxy in the management of 200 consecutive intracranial mass lesions. Analysis of indications, benefits and outcome. Br J Neurosurg 1990;4:407-15. 98. Bennett. A stereotaxic apparatus for use in cerebral surgery. Br J Radiol 1960;33:343–51. 99. Blandy JP, Greig CM, Gillam SJ, Williams DI. Lives of the fellows of the Royal College of Surgeons of England: 1997–2002: vol. 9 with a cumulated index to vol. 1–8. London: Royal College of Surgeons of England; 2005. 100. Eljamel MS, Forster A, Tulley M, Matthews K. Staged functional neurosurgery using image fusion: electronic atlas and microelectrode recording at Dundee. Stereotact Funct Neurosurg 1999;73:140-2. 101. Pell MF, Thomas DG. The initial experience with the Cosman-Roberts-Wells stereotactic system. Br J Neurosurg 1991;5:123-8. 102. Clarke RH. Part II: Atlas of the frontal sections of the cranium and brain of the rhesus monkey. Baltimore, MD: Johns Hopkins; 1920. 103. Clarke RH, Henderson EE. Atlas of photographs of sections of the frozen cranium and brain of the cat (Felis Domestica). J Psychol Neurol 1912;18:391-409. 104. Spiegel EA, Wycis HT, Baird HW. Studies in stereoencephalotomy. I. Topical relationships of subcortical structures to the posterior commissure. Confin Neurol 1952;12:121-33. 105. Schaltenbrand G, Bailey P. Introduction to stereotaxis with an atlas of the human brain. Stuttgart: Thienne; 1959. 106. Talairach J, David M, Tournoux P, Corredor H, Krasina T. Atlas d’Anatomie Stereotaxique. Paris: Masson; 1957. 107. Andrew J, Watkins ES. Stereotactic surgery. A stereotaxic atlas of the human thalamus. Baltimore, MD: Williams & Wilkins; 1969. 108. Afshar F, Watkins ES, Yap JC. Stereotaxic atlas of the human brainstem and cerebellar nuclei: a variability study. New York: Raven Press; 1978. 109. Mazzone P, Insola A, Lozano A, Galati S, Scarnati E, Peppe A, Stanzione P, Stefani A. Peripeduncular and pedunculopontine nuclei: a dispute on a clinically relevant target. Neuroreport 2007;18:1407-8. 110. Zrinzo L, Zrinzo LV, Hariz M. The pedunculopontine and peripeduncular nuclei: a tale of two structures. Brain 2007;130:e73; author reply e74. 111. Corsellis JA. Individual variation in the size of the tentorial opening. J Neurol Neurosurg Psychiatry 1958;21:279-83.

8

112. Watkins ES. On making stereotactic atlases. In: Gildenberg PL, Tasker RR, editors. Textbook of stereotactic and functional neurosurgery. New York: McGraw Hill; 1998. p. 235-6. 113. Cotzias GC, Van WM, Schiffer LM. Aromatic amino acids and modification of parkinsonism. N Engl J Med 1967;276:374-9. 114. Petrik V, Apok V, Britton JA, Bell BA, Papadopoulos MC. Godfrey Hounsfield and the dawn of computed tomography. Neurosurgery 2006;58:780-7; discussion 780-7. 115. Ambrose J, Gooding MR, Richardson AE. The Lancet – saturday II october 1975. Sodium iothalamate as an aid to diagnosis of intracranial lesions by computerised transverse axial scanning. Lancet 1975;2:669-74. 116. Ambrose J. CT scanning: a backward look. Semin Roentgenol 1977;12:7-11. 117. Ambrose J, Hounsfield G. Computerized transverse axial tomography. Br J Radiol 1973;46:148-9. 118. Hounsfield GN. Historical notes on computerized axial tomography. J Can Assoc Radiol 1976;27:135-42. 119. Hounsfield GN. Computed medical imaging. Science 1980;210:22-8. 120. Hitchcock E. Stereotactic-computerized tomography interface device. Appl Neurophysiol 1987;50:63-7. 121. Leksell L. A stereotaxic apparatus for intracerebral surgery. Acta Chir Scand 1949;99:229-33. 122. Leksell L. The stereotaxic method and radiosurgery of the brain. Acta Chir Scand 1951;102:316-9. 123. Rowe JG, Radatz MW, Walton L, Kemeny AA. Changing utilization of stereotactic radiosurgery in the UK: the Sheffield experience. Br J Neurosurg 2002;16:477-82. 124. Benabid AL, Pollak P, Louveau A, Henry S, de Rougement J. Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Appl Neurophysiol 1987;50:344-6. 125. Laitinen LV, Bergenheim AT, Hariz MI. Leksell’s posteroventral pallidotomy in the treatment of Parkinson’s disease. J Neurosurg 1992;76:53-61. 126. Aziz TZ, Adams CB. Neurosurgery at the radcliffe infirmary, Oxford: a history. Neurosurgery 1995;37:505-10. 127. Bergman H, Wichmann T, DeLong MR. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 1990;249:1436-8. 128. Aziz TZ, Peggs D, Sambrook MA, Crossman AR. Lesion of the subthalamic nucleus for the alleviation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)induced parkinsonism in the primate. Mov Disord 1991;6:288-92. 129. Aziz TZ, Peggs D, Agarwal E, Sambrook MA, Crossman AR. Subthalamic nucleotomy alleviates parkinsonism in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-exposed primate. Br J Neurosurg 1992;6:575-82.

93

94

8

History of stereotactic surgery in great britain

130. Parkin S, Nandi D, Giladi N, Joint C, Gregory R, Bain P, Scott R, Aziz TZ. Lesioning the subthalamic nucleus in the treatment of Parkinson’s disease. Stereotact Funct Neurosurg 2002;77:68-72. 131. Parkin SG, Gregory RP, Scott R, Bain P, Silburn P, Hall B, Boyle R, Joint C, Aziz TZ. Unilateral and bilateral pallidotomy for idiopathic Parkinson’s disease: a case series of 115 patients. Mov Disord 2002;17:682-92. 132. Liu X, Rowe J, Nandi D, Hayward G, Parkin S, Stein J, Aziz T. Localisation of the subthalamic nucleus using radionics image Fusion? and Stereoplan? combined with field potential recording: a technical note. Stereotact Funct Neurosurg 2001;76:63-73. 133. Aziz TZ, Nandi D, Parkin S, Liu X, Giladi N, Bain P, Gregory RG, Joint C, Scott RB, Stein JF. Targeting the subthalamic nucleus. Stereotact Funct Neurosurg 2002;77:87-90. 134. Aziz T, Torrens M. CT-guided thalamotomy in the treatment of movement disorders. Br J Neurosurg 1989;3:333-6. 135. Pereira EA, Green AL, Nandi D, Aziz TZ. Deep brain stimulation: indications and evidence. Expert Rev Med Devices 2007;4:591-603. 136. Munro-Davies LE, Winter J, Aziz TZ, Stein JF. The role of the pedunculopontine region in basal-ganglia mechanisms of akinesia. Exp Brain Res 1999;129:511-7. 137. Nandi D, Aziz TZ, Giladi N, Winter J, Stein JF. Reversal of akinesia in experimental parkinsonism by GABA antagonist microinjections in the pedunculopontine nucleus. Brain 2002;125:2418-30. 138. Jenkinson N, Nandi D, Miall RC, Stein JF, Aziz TZ. Pedunculopontine nucleus stimulation improves akinesia in a parkinsonian monkey. NeuroReport 2004;15:2621-4. 139. Nandi D, Jenkinson E, Miall C, Stein JF, Aziz TZ. Pedunculopontine nucleus. J Neurosurg 2004;100:978-9; author reply 979. 140. Kleiner-Fisman G, Herzog J, Fisman DN, Tamma F, Lyons KE, Pahwa R, Lang AE, Deuschl G. Subthalamic nucleus deep brain stimulation: summary and metaanalysis of outcomes. Mov Disord 2006;21 Suppl 14: S290-304. 141. Stefani A, Lozano AM, Peppe A, Stanzione P, Galati S, Tropepi D, Pierantozzi M, Brusa L, Scarnati E, Mazzone P. Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson’s disease. Brain 2007;130(6):1596-1607. 142. Schupbach WM, Chastan N, Welter ML, Houeto JL, Mesnage V, Bonnet AM, Czernecki V, Maltete D, Hartmann A, Mallet L, Pidoux B, Dormont D, Navarro S, Cornu P, Mallet A, Agid Y. Stimulation of the subthalamic nucleus in Parkinson’s disease: a 5 year follow up. J Neurol Neurosurg Psychiatry 2005;76:1640-4. 143. Rodriguez-Oroz MC, Obeso JA, Lang AE, Houeto JL, Pollak P, Rehncrona S, Kulisevsky J, Albanese A,

144.

145.

146.

147.

148.

149.

150.

151.

152.

153.

154.

155.

Volkmann J, Hariz MI, Quinn NP, Speelman JD, Guridi J, Zamarbide I, Gironell A, Molet J, Pascual-Sedano B, Pidoux B, Bonnet AM, Agid Y, Xie J, Benabid AL, Lozano AM, Saint-Cyr J, Romito L, Contarino MF, Scerrati M, Fraix V, Van Blercom N. Bilateral deep brain stimulation in Parkinson’s disease: a multicentre study with 4 years follow-up. Brain 2005; 128:2240-9. Liu X, Miall RC, Aziz TZ, Palace JA, Stein JF. Distal versus proximal arm tremor in multiple sclerosis assessed by visually guided tracking tasks. J Neurol Neurosurg Psychiatry 1999;66:43-7. Liu X, Yianni J, Wang S, Bain PG, Stein JF, Aziz TZ. Different mechanisms may generate sustained hypertonic and rhythmic bursting muscle activity in idiopathic dystonia. Exp Neurol 2006;198:204-13. Wang S, Liu X, Yianni J, Green AL, Joint C, Stein JF, Bain PG, Gregory R, Aziz TZ. Use of surface electromyography to assess and select patients with idiopathic dystonia for bilateral pallidal stimulation. J Neurosurg 2006;105:21-5. Pereira EA, Green AL, Bradley KM, Soper N, Moir L, Stein JF, Aziz TZ. Regional cerebral perfusion differences between periventricular grey, thalamic and dual target deep brain stimulation for chronic neuropathic pain. Stereotact Funct Neurosurg 2007;85:175-83. Kringelbach ML, Jenkinson N, Green AL, Owen SL, Hansen PC, Cornelissen PL, Holliday IE, Stein J, Aziz TZ. Deep brain stimulation for chronic pain investigated with magnetoencephalography. Neuroreport 2007;18:223-8. Muthusamy KA, Aravamuthan BR, Kringelbach ML, Jenkinson N, Voets NL, Johansen-Berg H, Stein JF, Aziz TZ. Connectivity of the human pedunculopontine nucleus region and diffusion tensor imaging in surgical targeting. J Neurosurg 2007;107:814-20. Aravamuthan BR, Muthusamy KA, Stein JF, Aziz TZ, Johansen-Berg H. Topography of cortical and subcortical connections of the human pedunculopontine and subthalamic nuclei. Neuroimage 2007;37:694-705. Green AL, Wang S, Owen SL, Paterson DJ, Stein JF, Aziz TZ. Controlling the heart via the brain: a potential new therapy for orthostatic hypotension. Neurosurgery 2006;58:1176-83; discussion 1176‐83. Green AL, Wang S, Owen SL, Xie K, Bittar RG, Stein JF, Paterson DJ, Aziz TZ. Stimulating the human midbrain to reveal the link between pain and blood pressure. Pain 2006;124:349-59. Yianni J, Bain P, Giladi N, Auca M, Gregory R, Joint C, Nandi D, Stein J, Scott R, Aziz T. Globus pallidus internus deep brain stimulation for dystonic conditions: a prospective audit. Mov Disord 2003;18:436-42. Owen SL, Green AL, Nandi DD, Bittar RG, Wang S, Aziz TZ. Deep brain stimulation for neuropathic pain. Acta Neurochir Suppl 2007;97:111-16. Kitchen ND, Thomas DG. Minimally invasive stereotaxy: clinical use of the Gill-Thomas-Cosman (GTC)

History of stereotactic surgery in great britain

156.

157.

158.

159.

160.

161.

162.

repeat stereotactic localiser. Minim Invasive Neurosurg 1994;37:61-3. Sofat A, Kratimenos G, Thomas DG. Early experience with the Gill Thomas locator for computed tomographydirected stereotactic biopsy of intracranial lesions. Neurosurgery 1992;31:972-4. Gill SS, Patel NK, Hotton GR, O’Sullivan K, McCarter R, Bunnage M, Brooks DJ, Svendsen CN, Heywood P. Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat Med 2003;9:589-95. Love S, Plaha P, Patel NK, Hotton GR, Brooks DJ, Gill SS. Glial cell line-derived neurotrophic factor induces neuronal sprouting in human brain. Nat Med 2005;11:703-4. Patel NK, Bunnage M, Plaha P, Svendsen CN, Heywood P, Gill SS. Intraputamenal infusion of glial cell line-derived neurotrophic factor in PD: a two-year outcome study. Ann Neurol 2005;57:298-302. Plaha P, Gill SS. Bilateral deep brain stimulation of the pedunculopontine nucleus for Parkinson’s disease. Neuroreport 2005;16:1883-7. Page RD, Miles JB. Validation of CT targeting for functional stereotaxis with postoperative magnetic resonance imaging. Br J Neurosurg 1994;8:461-7. Dervin JE, Miles J. A simple system for image directed stereotaxis. Br J Neurosurg 1989;3:569-74.

8

163. Dervin JE, Miles JB. Development of an analogue method to link stereotactic surgery to computed tomography. Neurochirurgia (Stuttg) 1984;27:162-5. 164. Dorward NL, Alberti O, Palmer JD, Kitchen ND, Thomas DG. Accuracy of true frameless stereotaxy: in vivo measurement and laboratory phantom studies. Technical note. J Neurosurg 1999;90:160-8. 165. Thomas DG, Kitchen ND. Stereotactic techniques for brain biopsies. Arch Dis Child 1993;69:621-2. 166. Kitchen ND, Lemieux L, Thomas DG. Accuracy in frame-based and frameless stereotaxy. Stereotact Funct Neurosurg 1993;61:195-206. 167. Thomas DG, Nouby RM. Experience in 300 cases of CTdirected stereotactic surgery for lesion biopsy and aspiration of haematoma. Br J Neurosurg 1989;3:321-5. 168. Thomas DG, Anderson RE, du Boulay GH. CT-guided stereotactic neurosurgery: experience in 24 cases with a new stereotactic system. J Neurol Neurosurg Psychiatry 1984;47:9-16. 169. Powell M, Kitchen N. The development of neurosurgery at the National Hospital for Neurology and Neurosurgery, Queen Square, London, England. Neurosurgery 2007;61:1077-90; discussion 1090. 170. Gildenberg PL. Stereotactic surgery: the early years (comment). Neurosurgery 2004;55:1214.

95

12 History of Stereotactic Surgery in India P. K. Doshi

Ancient Indian Literature The earliest reference to any functional neurosurgery in world could be found in Indian mythology script Shiva Purana (http://is1.mum.edu/vedicreserve/puran.htm). It reflects a transplantation of elephant head on a human being (Ganesha). Ganesha – the elephant-deity riding a mouse – has become one of the most common mnemonics for anything associated with Hinduism. The son of Shiva and Parvati, Ganesha has an elephantine countenance with a curved trunk and big ears, and a huge pot-bellied body of a human being. (> Figure 12-1) He is worshipped as Lord of success and destroyer of evils and obstacles. He is also worshipped as the god of education, knowledge, wisdom, and wealth. The story of the birth of this zoomorphic deity, as depicted in the Shiva Purana, goes like this: Once goddess Parvati, while bathing, created a boy out of the dirt of her body and assigned him the task of guarding the entrance to her bathroom. When Shiva, her husband returned, he was surprised to find a stranger denying him access, and struck off the boy’s head in rage. Parvati broke down in utter grief and to soothe her, Shiva sent out his squad (gana) to fetch the head of any sleeping being who was facing the north. The company found a sleeping elephant and brought back its severed head, which was then attached to the body of the boy. Shiva restored its life and made him the leader (pati) of his troop, hence his name ‘‘Ganapati.’’ Shiva also bestowed a boon that people would worship him and invoke his name before undertaking any venture. #

Springer-Verlag Berlin/Heidelberg 2009

This narration highlights two important aspects of functional neurosurgery. One is the reproduction of a human being from dermis derived stem cell (‘‘created a boy out of the dirt of her body’’) and second, the ultimate aim/ achievement that could ever happen – ‘‘whole head transplant.’’ In another epic, it is documented that in 1800 BC, Jivaka (physician to the Lord Buddha) removed intracranial mass lesion through trephination.

Development of Stereotactic Surgery Neurosurgery in India is a post World War II development, resulting from the keen desire of the new rulers of independent India, that the country should keep up with all the modern advances in every field of Neurosurgery [1]. It is interesting to note that many of the pioneers of Indian neurosurgery were exposed to stereotactic and functional neurosurgery, during their training abroad, which helped them to develop stereotactic neurosurgical specialty parallel with the international advances. Stereotactic surgery developed in parallel across several centers in India. In this chapter, the development of each subset of functional neurosurgery is described separately along with the contributions of each center, rather than following the chronology of date. Most important references have been included but these are not necessarily all encompassing.

156

12

History of stereotactic surgery in india

. Figure 12-1 Lord Ganesha (Elephant God)

In the 1940s bold pioneers like Chintan Nambiar, a surgeon at Stanley medical college, Madras, used to perform freehand stereotactic lesions by using a template in the temporal region. While mentioning this in an oration, the pioneering stereotactic surgeon B Ramamurthi quotes ‘‘The surgeon was bold and the patients bolder.’’ He performed 74 cases of chemopallidectomy using this free hand technique, out of which 27 had excellent results [2]. The first neurosurgical set up was established at the Christian Medical College (CMC), Vellore, in Tamilnadu, by Jacob Chandy. Chandy had obtained 2 years of training under Wilder Penfield at the Montreal Neurological Institute (MNI). In January 1949, equipped with neurosurgical equipments brought from Canada and an EEG machine, Chandy started the neurosurgical unit at CMC. He started with ten beds spread across medical and surgical wards. In 1950, he

was joined by Baldev Singh, a neurologist. In 1962, CMC acquired the Bertrand stereotactic guide, with the help of which they performed surgeries for Parkinson’s disease and epilepsies. Later in 1987, KV Mathai procured BRW frame. CMC became an established stereotactic unit, where till date around 1,800 stereotactic biopsies, 400 stereotactic craniotomies, 100 functional neurosurgical procedures, and 700 radiosurgical procedures have been performed. Vedantam Rajashekar, the present Head of the Department of Neurosurgery, and past president of the Indian Society of Stereotactic and Functional Neurosurgery, has been conducting stereotactic workshop to train young neurosurgeons [1]. Following on the heels of the department at Vellore was that at the Madras Medical College and Government Hospital; with the joining of Ramamurthi, in October 1950. Ramamurthi started his neurosurgical training with Rowbotham, in Newcastle upon Tyne, England. Subsequently he visited numerous centers across Europe and USA to gain wider experience. He also visited MNI and observed Rasmussen’s and Penfield’s work. Ramamurthi started neurosurgical unit with four beds which were increased to ten after 18 months [1]. Inspired by Irving Cooper’s use of an inflatable balloon to make lesions in pallidum for the treatment of Parkinson’s diseases, V Balasubramaniam and Ramamurthi performed surgeries using Cooper’s balloon (1962) [3]. Under radiological guidance a balloon was introduced and left in place for 48 h. This was followed by alcohol ablation. After performing surgeries on 12 patients of movement disorders, they were discouraged with the results. Import restrictions and bureaucratic hurdles made further imports of these balloons difficult and hence they gave up this method. In 1960 Ramamurthi received an invitation for dinner with the Governor of Hyderabad, General Shrinagesh (> Figure 12-2). It happened that the Governor was suffering from Parkinson’s disease and had undergone unilateral lesion in London by Lawrence Walsh at Atkinson Morley Hospital.

History of stereotactic surgery in india

12

. Figure 12-2 Ramamurthi having dinner with, General Shrinagesh (Black Suit), Governor of Andhra Pradesh

He asked Ramamurthi if such facilities are available in India as he had started experiencing symptoms on the opposite side. Ramamurthi explained that though he had the necessary expertise, the equipments were not available. In those days it was very difficult to import any equipment or obtain foreign exchange to travel abroad. General Shrinagesh immediately called up the Prime Minister of India, Pandit Jawaharlal Nehru; it was 11 PM. The Prime Minister immediately agreed to Shrinagesh’s suggestion to bring in Lawrence Walsh and Denis Williams (Neurologist) from England to conduct a workshop and training for movement disorders surgery. They also obtained permission for Walsh to leave his equipment behind after the workshop. Walsh and Williams came and stayed in Madras for 3 weeks during which they performed 40 surgeries and 30 neuroscientists took advantage of their expertise (> Figure 12-3). On completion of the program as decided, they left the Leksell stereotactic apparatus and the lesion generator back in Madras [4]. This was a major impetus and from there on Madras became a leading stereotactic center where more than 1,700 procedures were performed between 1959 and 1975 (> Table 12-1). Presently very little work is being

done at this center after Ramamurthi and his team retired from the Madras Medical College. In 1970, S Kalyanaraman, a young neurosurgeon in Ramamurthi’s team from the Madras Medical College, reported simultaneous use of two stereotactic apparatus on the same patient. He used the Leksell stereotactic equipment in combination with the Sehgal stereotactic equipment to perform simultaneous targeting of intracranial structures. Sehgal’s stereotactic equipment is a compact, burr hole based stereotactic device designed by Arjun Sehgal in India. The Leksell frame was used to align Sehgal’s apparatus to the target on one side and on the other it was used to approach the target. The purpose was to obtain simultaneous recording from the thalamus, thus reducing the operative time. They also observed that the number of X-rays required to localize the targets were reduced [5,6]. RM Varma started a neurosurgical unit in the (then) All India Institute of Medical Health, Bangalore, in 1958. Varma’s efforts led to the formation of the National Institute of Mental Health and Neurosciences (NIMHANS) out of this unit [7]. Varma was trained in Bristol and started performing lesions for Parkinson’s disease using a unique free hand technique, through

157

158

12

History of stereotactic surgery in india

. Figure 12-3 Lawrence Walsh, Chief Nurse, Ramamurthi and Dennis Williams

. Table 12-1 Stereotactic Surgery at Madras Medical College (1959– 1975) Thalamotomy Amygdalotomy Hypothalamotomy Cingulumotomy Basofrontal tractotomy Dentatectomy Leucotomy Thalamolaminotomy Capsulotomy Pulvinotomy Mesencephalc reticulotomy Hypophysectomy

858 480 122 143 56 73 5 11 16 4 2 2

foramen ovale. Later on in 1980s, they obtained the Leksell stereotactic equipment and recently a gamma knife unit. HM Dastur, started stereotactic surgery at King Edward Memorial (KEM) Hospital, Bombay (Mumbai) in 1959. The initial surgeries were performed using Oliver’s guide. Narabayashi visited KEM hospital in 1962 and lent the design of his stereotactic frame for fabricating a local frame on similar lines. Later on in 1975, Dastur joined Jaslok Hospital, Bombay (Mumbai), where he continued to perform stereotactic surgery using

a Reichert-Mundinger frame. In another center at Bombay Hospital, SN Bhagwati started stereotactic surgery with Mckinney’s apparatus from 1962 and this was replaced by Leksell’s frame in 1964. Multiple centers started practicing stereotactic surgery in the 1970s. These include Post Graduate Institute of Medical Education and Research (PGIMER), Chandigarh (1974), with Mckinney frame, All India Institute of Medical Sciences (AIIMS), New Delhi (1977), with Leksell frame and Shri Chitra Tirunal Institute for Medical Sciences and Technology (SCTIMST) with Leksell frame [2,8]. In 1991 Mr. Bose, an engineer and Apte, a neurosurgeon from Pune, developed an indigenous arc centered stereotactic apparatus. Three revisions have been made to this initial model, which is now compatible for CT and MRI guided procedures. They followed this by manufacturing a radiofrequency lesion generator in 1996. The prices of these equipments are considerably lower than standard stereotactic frames and hence have become popular for performing biopsies and other stereotactic procedures. Presently 40 neurosurgical units have stereotactic equipment and

History of stereotactic surgery in india

they perform various levels of stereotactic procedures from biopsy to functional neurosurgery. The Indian Society of Stereotactic and Functional Neurosurgery was formed in 1997. Its first meeting was held in Delhi with Balasubramaniam as president and Rajashekar as Secretary. In 2007 the tenth meeting of the society was held in Kolkata. This is a rapidly expanding society with the current membership of more than 100 members. Stereotactic radiosurgery was first introduced in India at the Apollo Hospitals, Chennai, using Linac based X-knife system. Linac based radiosurgery is offered at multiple centers including Bombay Hospital and Jaslok Hospital, Mumbai. Gamma Kinfe was introduced at Hinduja Hospital, Mumbai, in 1997 [9]. This was soon followed by similar units at AIIMS and VIMHANS in New Delhi, and later on at other centers including Vellore, NIMHANS, R&R (Army Hospital, New Delhi), PGIMER (Chandigarh) etc.

Epilepsy Surgery In the early days of stereotactic and functional neurosurgery the enthusiasm of the neuroscientists could not be contained. Virtually lesions were placed in every part of the brain for varied disorders ranging from epilepsy to psychiatric illness [10]. To further understand the development drivers of these surgeries, we need to look into India’s social and economical background of that period. A recent (2006) survey (http://www. prb.org/Articles/2006/CommunityBasedHealth InsuranceShowsPromiseinIndia.aspx) showed that only 11% of Indian population had some kind of health insurance, this could not have been more than 2–4% in 1960s. Thus the medical treatment had to be funded by the patient themselves or they had to use government or municipal hospitals to treat them. Though these hospitals were supposed to be providing free medical treatment, the medicines (especially the expensive ones)

12

had to be purchased by the patient. Paradoxically the cost of surgeries in these hospitals was far less than prolonged medical treatment. In a report on epilepsy research, Mathai [11] mentions that follow-up studies indicated that where the person was receiving more than two drugs the cost of the therapy would come >2 $/month and only 10–15% of the patients had the resources to afford this. Hence in developing countries financial insufficiency formed an added indication for surgical therapy in the control of seizures. Chandy, who had trained at the MNI, started epilepsy surgery in CMC, Vellore in 1949. He was joined by Baldev Singh, a neurologist, who had interest in epilepsy and was equipped with an EEG machine to diagnose and manage epilepsy. Singh and Chandy [12] in an exhaustive study of delta waves in 800 EEG records at CMC, commented on their characteristics and localizing value. Those were the days when EEG was the only non-invasive investigation for brain disorders (including tumors). During 1949–1990, 141 epilepsy surgeries were performed at CMC [13]. They performed topectomy and lobectomy for suprasylvian epilepsy; for temporal lobe epilepsy (TLE) the surgical procedures done were topectomy, temporal lobectomy with amygdalectomy, temporal lobectomy with amygdalohippocampectomy, and only amygdalectomy. Hemispherectomy was done for cases with multilobar epilepsy. Temporal lobe resections were done based on the scalp EEG, sphenoidal studies, neuropsychological assessment and the intraoperative ECoG and depth electrode studies. Total or near total seizure control was obtained in 53% patients and a satisfactory outcome in 20% patients. They found that mental retardation, pre operative scalp EEG and post excision electrocorticography were predictors of outcome. In Madras, Ramamurthi developed an excellent team. He along with Balasubramaniam, Kalyanaraman and Kanaka as neurosurgical colleagues; Arjundas, Jaganathan and later on Sayeed as neurological colleagues, Vriddhagirinathan the

159

160

12

History of stereotactic surgery in india

psychologist and Valmikinathan, neurochemist developed a comprehensive epilepsy surgical program. They reviewed the literature and noted that Falconer had obtained good results by standard temporal lobectomies in three fourth of the patients [14]. Narabayashi and Chitanondh had reported 50% seizure control and improvement in behavioral disorders in patients undergoing amygdalectomy. Ramamurthi felt that massive temporal lobectomy, only to ablate these medial structures, is a mutilating procedure. They treated complex partial seizures with proved medial temporal focus with stereotactic lesions rather than by a full temporal lobectomy [15–19]. They established the details of localization of epileptic focus by careful pre and postoperative observations of their neurological colleagues. In a paper published in 1979 [20], Ramamurthi shares his experience of 56 cases that he operated. The patients included, suffered from purely TLE, TLE with secondary generalization or TLE with focal seizures. EEG studies including sphenoidal and depth electrode recordings were performed prior to surgery. Based on these findings, stereotactic lesions of 600–800 m3, were made in the area of maximum abnormality. He found that 26 of the 56 patients became seizure free and eight cases required reoperation. He commented that this procedure was useful in patients who had bilateral TLE or contralateral previous temporal lobectomy, as it preserved the hippocampus and thus the memory. Mathai, in CMC Vellore, also performed amygdalectomy through a craniotomy for similar reasons. They performed intraoperative corticography and depth studies from amygdala to plan their surgical resections. They concluded that when the seizure discharges are from the cortex rather than amygdala, excision of the amygdala only reduces the intensity of cortical activity. However, when the epileptiform discharges are primarily from the amygdala, amygdalectomy alone might suffice; especially when an electrocorticographic seizure can be produced by stimulating the

amygdala [11]. In Bombay (Mumbai), at KEM hospital Dastur, assisted by neurologist Anil Desai, performed epilepsy surgery including temporal lobectomy and hemispherectomy. He continued his work after joining Jaslok Hospital, where he was assisted by Mrs. PN Wadia, neurophysiologist in performing epilepsy surgery. Corticography and depth recordings during the surgery were also performed. During 1960s depth electrodes and corticography were used routinely for epilepsy surgeries. Arjundas observed that the depth electrode supplements information obtained from scalp EEG in identifying the epileptogenic focus and also reveals foci not evident in scalp EEG records [21]. Kanaka and Balasubramaniam found that depth studies were useful in understanding the propagation of epileptic discharges. They found that depth electrode study along with electrocorticography also provided precise localization of the epileptic focus. They used this information for planning appropriate surgery [22]. Kalyanaraman had obtained PhD degree from Edinburgh, University on ‘‘Anatomical and Physiological studies on the internal capsule and adjacent diencephalic structures during human stereotaxy.’’ Based on his work and the observations of Gillingham [23], Kalyanaraman postulated that in an area in the posterior limb of the internal capsule, medial to the pyramidal tract where lie the corticospinal fibers that form the common pathway for the epileptic seizure. A bilateral internal capsulotomy should control clinical seizures without causing pyramidal signs and without producing electroencephalographic improvement. To test this hypothesis, they performed bilateral internal capsulotomy on seven patients with intractable grand mal epilepsy. They had good outcome (comparable to Engel grade I and II) in three patients, considerable reduction in seizure frequency in one and poor outcome in two. One patient died of pneumonia postoperatively. None of these patients had significant permanent morbidity [24,25].

History of stereotactic surgery in india

Mathai postulated that in patients suffering from generalized seizures or focal seizures arising from significant (eloquent) cortical areas, which cannot be excised without producing serious neurological deficit, interruption of propagation pathways may modify the frequency and pattern of the seizures. They performed stereotactic lesioning of ansa and fasciculus lenticularis. Bertrand stereotactic guide was used and the target chosen was 1 cm behind AC and 1.5 cm lateral. A leucotome was used to make a lesion of 0.5–0.8 cm. Scalp and depth EEG recordings were obtained during this stage. They had variable results, ranging from good seizure control to reduction in seizure frequency and severity. They concluded that because of the multiple propagation pathways in epilepsy these procedures may only temporarily modify the clinical seizure pattern. However, in seizures where the frequency is once a day or more such procedures are of value. Destruction of ansa and fasciculus lenticularis bilaterally for generalized cerebral seizures and unilaterally for focal cortical seizures seems to alleviate, although not fully, the intensity and frequency of seizures [26]. Few epilepsy surgeries were performed during 1970–1990. Radhakrishnan, epileptologist, started an epilepsy surgery program at the SCTIMST. This was a complete program with facilities for invasive recording, neuropsychology, video EEG and nuclear medicine. Their initial focus was on temporal lobe epilepsy. From March 1995 through February 2002, they performed 394 epilepsy surgeries, 370 of them were anterior temporal lobectomy with amygdalohippocampectomy for refractory temporal lobe epilepsy. They reported 78% seizure freedom at 2 years follow-up [27]. Epilepsy surgery was started in AIIMS, by VP Singh [28], at Jaslok Hospital by P Doshi and at Hinduja Hospital by CE Deopujari and BK Misra in the late 1990s. All these centers have facilities of state of the art neuroradiology, neurophysiology

12

(including prolonged video EEG), nuclear medicine departments for SPECT and PET scans, neuropsychologist, epileptologist and functional neurosurgeon.

Movement Disorders Surgery Movement disorders surgery has had the most colorful history in any account of functional neurosurgery. This is true for India as well. Enterprising neurosurgeons used varied techniques from free hand technique to frame based systems, unilateral and bilateral lesions, even simultaneous bilateral lesions; alcohol to radiofrequency lesioning and from pallidum to field of Forel, to ameliorate movement disorders. Balasubramaniam and Ramamurthi started performing chemopallidectomy using Cooper’s balloon in 1962 as mentioned earlier [3]. From 1964 they used the Leksell’s apparatus to perform thermal lesions for movement disorders [29]. Kalyanaraman, performed bilateral simultaneous thalamotomies in patients with various movement disorders. They observed that the complication rate was acceptable and no greater than staged procedures in patients with advanced Parkinson’s disease. In patients with bilateral intention tremors this formed a good surgical option as it avoided double hospitalization [30]. Using Sehgal’s stereotactic apparatus he used to perform bilateral simultaneous recordings as described earlier. During surgery an opaque marker was introduced into the site of the lesion. Immediate postoperative X-rays were taken and the exact location of the lesion was charted with the help of the atlas prepared by Schaltendrand and Bailey. This served not only to assess the accuracy of lesion placement but also to correlate the result of surgery with the site of the lesion. They noted minor differences in the anatomical calculations of deep brain structures in different races and groups [31].

161

162

12

History of stereotactic surgery in india

Though in 1970s, the number of surgeries for Parkinson’s disease started decreasing, due to the cost constraints of prolonged Levodopa therapy excellent surgical benefits (especially for unilateral disease) Madras group continued to perform surgeries for Parkinson’s disease. Another unique area of interests was the treatment for cerebral palsy. Following the work of Narabayashi [32], Balasubramaniam and his colleagues operated on a large number of cerebral palsy patients. As their experience evolved they chose different targets depending on the predominant symptom complex. For Rigidity they made a lesion in the area below the ventrolateral nucleus (VL); for dyskinesias they used variety of targets including the ventralis intermedius nucleus (VIM), the centromedian nucleus (CM) and the dentate nucleus of the cerebellum. As most of these surgeries were done under general anesthesia verification of the electrode placement by stimulation, as done in Parkinson’s disease was not possible. Stimulation was still done to exclude electrode placement in the corticospinal tract [33]. They later on introduced stereotactic dentatectomy for patients with predominant spasticity. They found that VL and sub VL lesions were effective for rigidity, whereas for patients with a mix of rigidity and spasticity these lesions had to be supplemented by dentatectomy. Patients with sensory induced involuntary movements benefited from centromedian thalamotomy [34]. For severe hyperkinetic disorders, Kanaka found hypothalamotomy to play a distinct role in their management. She observed that it works because the area destroyed forms part of the limbic system. It seemed to be more on the ‘‘effector’’ side. It does not cause any morbidity. In the management hyperkinetic behavior disorders the first target to be destroyed must be the amygdaloid nucleus. If this operation fails, then hypothalamotomy may be done as the next operation [35]. Varma (1964) in Bangalore developed a free hand technique of lesioning the thalamus for

Parkinson’s disease. He modified the technique of Arthur Ecker and Theoder Perl [36] for this surgery. The technique involved use of two needles, outer 19G, to cannulate the foramen ovale; and the inner, 26G to perform chemothalamotomy. The outer needle had a slight curve at the end to help direct the inner needle to the desired position (> Figure 12-4). Varma used external landmarks to do away with ventriculography. He used lead pellets placed on the external canthus of the eye and in the internal auditory meatus to serve as markers. Lateral and AP radiographs were obtained after the introduction of the needle. A topograph was created outlining the above landmarks in relation to the venterolateral thalamus (based on an atlas). This was then overlain on the lateral x-ray and the distance between the needle and the target obtained. Appropriate radiographic and anthropometric corrections were applied to calculate the relationship of the needle to the target and the final position of needle adjusted. Varma notes that in many patients the tremor used to get arrested when the needle reached the target. This was then followed by chemothalamotomy with absolute alcohol [37]. His work was later on reviewed with MRI imaging of the patients operated, by . Figure 12-4 Varma’s Foramen Ovale ‘‘Thalamotomy’’ for PD. Outer and inner needle seen in situ, with cranial landmarks outlined

History of stereotactic surgery in india

Uday Muthane [38,39]. Muthane analyzed the site of the lesion by MRI and, in one case, postmortem examination. He noted that the lesion was actually placed 1.5 cm below the thalamus and it coincided with the subthalamic nucleus. Stereotactic surgery was performed initially at CMC, Vellore by the free hand technique and later from 1961 onwards using Bertrand’s frame. Parkinson’s disease and dystonia were the main indications. The initial target used was globus pallidum, which was, later on changed to the thalamus. The free hand technique involved localizing the foramen of Monro using pneumoenchephalogram and pallidal target was calculated based on stereotactic atlas derived coordinates. AP and lateral radiographs were used for localization. The lesions were made using absolute alcohol in incremental methods whilst checking for neurological deficits (Mathai KV, personal communication). In Bombay (Mumbai), Dastur started performing lesions in thalamus, pallidum and field of Forel for dystonia at the KEM hospital in 1959 (Dastur HM, personal communication). Desai, neurologist associated with KEM neurosurgical department, visited Narabayashi in 1962, to assist Dastur in performing movement disorders surgery. The program received further impetus following Narabayashi’s visit. Dastur recounts a very interesting experience. They planned to perform a Cooper’s lesion for a patient with severe ‘‘hyperkinesis.’’ Following surgery, the patient had a remarkable improvement. However, on postoperative x-ray analysis they found that their lesions were not in the intended area but the lesions were more in the ventrolateral thalamus above the CA-CP plane. Gajendra Sinh, neurosurgeon at the Jaslok Hospital, used to call this a KEM lesion. The lesions were made using myodil and wax (> Figure 12-5). In 1974 Sinh invited Laitinen to visit Jaslok Hospital. Laitinen demonstrated his pallidotomy operations, which were then followed up by Sinh. After the 1980s movement disorders surgery

12

. Figure 12-5 Notings of ‘‘KEM thalamotomy’’ by Dastur

almost stopped following remarkable improvement in medical management. In another unit in Bombay (Mumbai), Bhagwati and his colleagues performed thalamotomies for Parkinson’s disease in 110 cases. They were also convinced about the efficacy of bilateral lesions and 30 of these patients had undergone bilateral lesions. They reported an interesting observation of reactivation of successfully abolished tremors on thalamic stimulation whilst performing surgery for the second side in Parkinson’s disease. In five of the thirty patients who underwent staged (minimum interval 6 months) bilateral thalamotomy, tremors recurred on the side of the second thalamotomy, i.e., on the ipsilateral side. In three patients, they performed a repeat lesion for the control of these tremors, but the patients had a rather stormy convalescence and developed drowsiness, confusion,

163

164

12

History of stereotactic surgery in india

dysarthria with one of them developing pseudobulbar palsy, in the next two patients simultaneous bilateral lesions were not made. The recurrent tremors persisted in these two patients [40]. Kalyanaraman also had similar experience in patients undergoing bilateral thalamotomy. Bhagwati earlier used diathermy to make lesions but later on switched over to cryo lesioning [41]. Once again, like other places in the world, interest in Parkinson’s disease surgery waned after the introduction of Levodopa. Surgery for movement disorders surgery was revived in 1997. Doshi after his training in Europe started performing pallidotomy. However, within a short period (1998) he switched over to deep brain stimulation surgeries [42]. He and his colleagues observed that STN DBS can produce depression in an occasional patient [43], which was later on accepted as an important side effect in almost 8–18% of STN DBS patients [44,45]. SCTIMST also started performing pallidotomy and deep brain stimulation around the same time. Presently movement disorder surgery is being performed in Mumbai, Hyderabad, Banglore, Trivandrum and Delhi.

Surgery for Chronic Pain Roy offered stereotactic cingulotomy for intractable terminal cancer pain. He used Oliver’s apparatus. The needle was positioned to produce a lesion 2–4 cm posterior to anterior tips of the ventricles and 2 cm in vertical height from above the ventricles. 0.1 ml of carbolic acid with myodil was used in making the lesion. The maximum relief was noted approximately for 2 months after the operation. After this period, the relief of pain was not complete and analgesics were again required. They advocated this surgery for terminally ill cancer patients [46]. Dorsal cordotomy was the preferred procedure in patients suffering from pain of incurable

malignancy in the lower half of the body. However, when the upper half of the body was involved intracranial targets were chosen. Ramamurthi [47] notes that intractable pain due to lesions other than malignancy was not often seen in Indian neurosurgical practice. The incidence of oropharyngeal cancer was very common in South India and advanced cases reported with intractable pain. In such cases section of the trigeminal or the glossopharyngeal nerve was fraught with grave risks especially due to deglutition difficulties with resultant risk of aspiration. Kalyanramana and Ramamurthi studied the neurophysiology of the sensory relay nucleus [48]. From the atlas of Schaltenbrand and Bailey [49] they calculated that the facial area of the sensory relay nucleus of the thalamus was centered on a point 4 mm in front of the center of the posterior commissure, 4 mm above the intercommissural line and 13 mm lateral to the midsagittal plane. Whereas, the termination of the quintothalamic tract into the sensory relay nucleus was calculated to be centered around a point 3 mm in front of the posterior commissure, on the intercommissural line and 10 mm lateral to the midsagittal plane. They used neurophysiological guidance to further refine their target localization. They noted that though sensory responses could be obtained from the internal capsule or other parts of thalamus, the threshold of this response was lowest when the electrode was in the sensory relay nucleus. They also found that microelectrode recordings showed evoked potentials from peripheral stimulation. They initially made large lesions of 8 mm, five times, in the first few patients. However, later on they made only one lesion of 8 mm in the sensory thalamus and an additional lesion in the quintothalamic tract region if pain relief was not adequate. As most of these patients suffered from terminal cancer, they died after a few months and had adequate pain relief till they lived. Two patients who had post herpetic neuralgia

History of stereotactic surgery in india

continued to have pain relief at a follow-up of 6 months [50]. They also performed cingulotomy and hypothalamotomy for pain relief [51].

Psychiatric Disorders Surgery There was a great interest and enthusiasm amongst Indian neurosurgeons in the field of psychiatric disorders surgery as early as 1940. Balkrishna Rao in Bangalore, performed prefrontal leucotomies on patients selected by Govindaswami [52]. BK Anand, a neurophysiologist, participated in the study of the role of the hypothalamus and limbic system in the regulation of feeding behavior conducted by John Fulton and JR Brobeck [53,54]. They discovered, what is since known as, the hypothalamic feeding center. On returning to India, he worked at the Lady Hardinge Medical College, New Delhi and later, at the Department of Physiology, AIIMS, New Delhi [55]. He introduced new experimental techniques and approaches for the study of brain and behavior in India. These include the methods of stereotactic placement of electrodes for making local electrolytic lesions, electrical stimulations, recording of depth EEG, evoked potentials and single unit potentials with microelectrodes and the usage of unanesthetized and free moving animals for behavioral experiments. Manchanda et al. [56] observed that electrical stimulation of perifornical regions of hypothalamus in the carnivore cat evoked different varieties of aggressive behavior: flight, defense, attack. These led other researchers and neurosurgeons to explore the vast field of psychiatric disorders surgery. During his training with Rowbotham, Ramamurthi used to visit St. Lukes Hospital at Middlesborough, where Rowbotham used to perform prefrontal leucotomies. He found that it was successful in more than 60% of the patients. He decided to undertake this upon return to India.

12

Ramamurthi found that the psychiatrists in South India were forward looking and readily referred cases for surgery [10]. For severe depression, Ramamurthi performed a stamp size lesion, extending from 0.7 to 3.0 cm from the midline and 0.8 to 2.8 cm in front of the tip of the anterior clinoid process in the subfrontal region using the diathermy [57]. There was an instantaneous improvement, with some patients describing that ‘‘a great load has been lifted off my chest.’’ Most patients benefitted [58]. In Obsessive Compulsive neurosis, lesions were made in the cingulum. The results were good and long lasting. In some patients, where the results were not as good as expected another lesion was made in the subfrontal region or the cingulum [59–61]. Another interesting indication for psychosurgery was drug addiction. Thirty two cases suffering from drug addictions (alcohol, morphine and pethidine) were operated by Balasubramaniam during 1970–1972. Surgery was done under general anesthesia. Stereotactic localization was performed using pneumoencephalography and carotid angiography. These investigations were essential to determine the thickness of the corpus callosum for making precise lesion in the cingulum, clearing the corpus callosum. The target was selected in line with the foramen of Monro, midway between the pericallosal and callosomarginal arteries. In the coronal plane, the center of the target was 7 mm from the midline. Destruction was done in all cases by injection of myodil, oil, and wax mixture prepared according to the formula of Narabayashi [62]. Both sides were done at one sitting. Postoperative x-rays were taken to confirm the accuracy of the lesion. Of the twenty eight cases followed up for more than 6 months, 22 had been addiction free [63]. Recounting his experience Ravi Ramamurthi says that he found that this was most effective for pethidine addicts. He also mentioned that it was only offered to the patients who were inclined to

165

166

12

History of stereotactic surgery in india

be weaned off their addiction but had failed. The cingulotomy would take away the affective part of their withdrawal symptoms. Balasubramaniam and his colleagues also performed stereotactic amygdalotomy for aggressive behavior in children and adults. Such behavior ranged from continuous severe violent acts towards others, pyromania, destructive tendencies, to episodic attacks of behavior disorders or severe degrees of restlessness. The aim of the operation was to destroy the amygdaloid nucleus or its connections so as to make the patient more manageable either with or without drugs. During 1964–1967, they performed 50 operations on 44 patients; most of them bilateral. The center of the amygdaloid nucleus was considered to be 4 mm in front of the apex of the temporal horn. Two reference points were taken. The first 18 mm below the CACP plane, 6 mm anterior to midcommisural plane and 22 mm from the midsagittal plane. The second reference point was 4–5 mm anterior to the apex of the temporal horn. The author’s preferred the second reference point. In case there was significant cortical atrophy, the first reference point was used. The lesion was made either by diathermy coagulation or Bertrand loop. Diathermy coagulation was done with an 8 mm. electrode, the area of destruction being approximately 200 m3. For the amygdaloid nucleus nine lesions were made. The total volume would be about 1,800 m3 which was slightly greater than the volume of the amygdaloid nucleus which is about 1,200 m3. The lesions made with Bertrand loop were much smaller measuring 500 m3. In 30 operations diathermy was employed and in 19 the Bertrand loop. In one operation both were used. They found that patients having aggressive behavior associated with epilepsy had a better outcome as compared to those suffering from post encephalitic illness aggression [64]. Another target of interest was the posterior hypothalamus. Stereotactic intervention into the posterior hypothalamus was noted to give

satisfactory results for controlling both aggressive, violent behavioral disorders and intractable pain. From the endocrinological point of view, this procedure activates the hypothalamic-hypophyseal axis only temporarily, without causing any serious dysfunctions [65]. Based on these observations Balasubramaniam and Kanaka performed hypothalamotomy on patients who failed to improve after amygdalotomy [66–68]. During the subsequent years, 522 surgeries were performed for aggressive behavior disorder, 402 were bilateral amygdalotomies, and 120 posteromedian hypothalamotomy [69].

Neural Transplantation Stimulated by the reports of A Bjorklund and GD Das at the first congress of the International Brain research organization held at Laussane, Switzerland in 1982, Gopinath (neuroanatomist), Tandon and Mahapatra (neurosurgeons) with Nayar and Mohan Kumar (neurophysiologist) set up a unit to study neural transplantation, with the help of the Department of Science and Technology. They studied neural transplants in rat and primates. Transplantation of embryonic neocortex was performed into cerebellum, lateral ventricle, third ventricle, striatum, hippocampus, tectum and the anterior chamber of the eye in rat. Behavioral and electrophysiological studies were carried out before and after transplantation. Transplantations were also performed in rhesus monkey’s striatum, neocortex and cerebellum for standardization. Parkinson’s disease model was produced in rhesus monkeys using MPTP. As it was difficult to maintain a bilateral Parkinson’s disease model, a unilateral disease model was created. After stabilizing the signs and symptoms for 4–12 weeks, they were grafted with fetal substantia nigra into the striatum using stereotactic techniques. Four monkeys were transplanted. Gopinath [70] notes that three of the four monkeys improved sufficiently to handle food

History of stereotactic surgery in india

while one had to be sacrificed due to complications [71]. Similar transplant program was also initiated at NIMHANS [72] in 1989 and at the post graduate institute of basic medical sciences, Madras [73,74]. Presently, various centers in Bangalore and Delhi are performing studies on Mesenchymal stem cell transplantation for Parkinson’s disease and spinal cord injury. Currently, India is experiencing a renaissance of stereotactic and functional neurosurgery. Imports of equipment has become easier and the present generation of neurosurgeons have the best of both the worlds; extensive clinical experience in India as well as advanced training in specific fields from various centers around the world. There is an increase in understanding and interest in developing India into a global health care provider. Realizing this, a large number of private hospitals have begun to invest in state-of-the-art equipment, thus providing an important platform for the development of this subspecialty.

Acknowledgment I would like to acknowledge the help of NH Wadia and Ravi Ramamurthi for critically reviewing the manuscript. Ravi Ramamurthi, RM Varma, Uday Muthane, KV Mathai, V Rajashekar, and HM Dastur for providing information and personal inputs.

References 1. Sridhar K. Prof. Ramamurthi: the legend and his legacy. Neurol India 2003;52:27-31. 2. Kak V. Neurosurgery. In: Pandya SK, editor. Neurosciences in India retrospect and prospect. New Delhi: The Neurological Society of India; 1989. p. 577-641. 3. Cooper IS. Chemopallidectomy: investigative technique in geriatric parkinsonism. Science 1955;121:217.

12

4. Ramamurthi B. The Governor and the Prime Minister. In: Ramamurthi B, editor. Uphill all the way – an autobiography. Chennai, India: Guardian Press; 2000. p. 206-16. 5. Kalyanraman S, Ramamurthi B. Two machine stereotaxy. Neurol India 1970;18(Suppl 1):53-5. 6. Kalyanaraman S, Ramamurthi B. Simultaneous bilateral stereotaxic lesions in the diencephalon. In: Second international symposium stereoencephalotomy, Copenhagen. Confin Neurol 1965;26:310-14. 7. Nadkarni TD, Goel A, Pandya SK. Neurosurgery in India. Neurol India 2002;48:332-5. 8. Bhatia R, Tandon PN, Banerji AK. Brain abscess – an analysis of 55 cases. Int Surg 1973;58(8):565-8. 9. Kannan V, Deopujari CV, Misra BK, Shetty P, Shroff MM, Pendse AM. Gamma-knife radiosurgery for trigeminal neuralgia. Australasian Radiol 1999;43(3): 339-41. 10. Ramamurthi B. Stereotactic surgery in India: the past, present and the future. Neurol India 2000;48:1-7. 11. Mathai K. Investigations into methods for the rehabilitation of persons disabled by convulsive disorders. Project no. 19-P-5113-F-OI. Division of International activities, Office of research demonstrations and training, social and rehabilitation service. Department of Health, Education and Welfare. Washington D.C: 20201. 12. Singh B, Chandy J. Electroencephalographic study of delta waves. Neurol India 1955;3:5-9. 13. Daniel RT, Chandy MJ. Epilepsy surgery: overview of 40 years of experience. Neurol India 1999;47(2):98-103. 14. Falconer F, Serafetinides FA. A follow up study of surgery in temporal lobe epilepsy. J. Neurol Neurosurg Psychiat 1963;26:300-7. 15. Balasubramaniam V, Kanaka TS. Stereotaxic surgery of the limbic system in epilepsy. Acta Neurochir suppl 1975;23:225-34. 16. Ramamurthi B. Stereotaxic surgery in temporal lobe epilepsy. Neurol India 1970;18:42-5. 17. Balasubramaniam V, Kalyanaraman S, Arjundas G, et al. Stereotaxic ablation of the irritable focus in temporal lobe epilepsy Confin Neurol 1970;32:316-21. 18. Kalyanaraman S, Sayeed ZA, Dharmapal N. Surgical treatment of epilepsy. In: Harris P, Mawdsley C, editor. Epilepsy, Proceedings of the Hans Berger centenary symposium. Edinburgh: Churchill Livingstone; 1974. p. 203-8. 19. Balasubramaniam V, Kanaka TS. Why hemispherectomy? Appl Neurophysiol 1975;38:197-205. 20. Ramamurthi B, Sayeed ZA, Rao DB. Stereotactic surgery of medial temporal structures in temporal lobe epilepsy. Neurol India 1979;27(4):192-5. 21. Arjundas G. Usefulness of depth electrode studies in epilepsies. In: Mani KS, Walker AE, Tandon PN, editors. Proceedings of national seminar on epilepsy. Bangalore:

167

168

12 22.

23.

24. 25.

26.

27.

28.

29. 30. 31.

32.

33.

34.

35.

36. 37.

38.

History of stereotactic surgery in india

Indian epilepsy association, Bangalore Chapter; 1976. p. 75-7. Kanaka TS, Balasubramaniam V. Cortical and depth electrode studies. Neurol India 1980;28:150-4; Mathai KV. Epilepsy – some epidemiological experimental and surgical aspects. Neurol India 1986;14:299-314. Gillingham FJ, Watson WS, Donaldson AA, Naughton JAL. The surgical treatment of parkinsonism. Brit Med J 1960;2:1395. Kalyanaraman S, Ramamurthi B. Stereotaxic surgery for generalized epilepsy. Neurol India 1970;18:34-41. Kalyanaraman S, Ramamurthi B. Stereotaxic capsulotomy for epilepsy. Proc Australian Assoc Neurol 1968;5: 311-12. Mathai KV, Taori GM. Stereotaxic destruction of ansa and fasciculus lenticularis in the control of seizures. Neurol India 1972;20(Suppl 2):169-74. Rao MB, Radhakrishnan K. Is epilepsy surgery possible in countries with limited resources? Epilepsia 2000;41: S31-4. Bhatia M, Singh VP, Jain S, et al. Epilepsy surgery in India: AIIMS experience. J Assoc Phys India 1999;47: 492-5. Balasubramaniam V, Ramamurthi B. Stereotactic surgery. Neurol India 1965;13(3):93-6. Kalyanaraman S, Ramamurthi B. Simultaneous bilateral stereotaxic lesions. Neurol India 1966;14(3):151-3. Kalyanaraman S, Ramamurthi B. The size of the third ventricle in British and Indian subjects. Neurol India Suppl 1:60-4. Narabayashi H. Physiological analysis of ventrolateral thalamotomy for rigidity and tremor. Confin Neurol 1965;26:264-8. Kanaka TS, Balasubramaniam V, Ramanujam PB, Ramamurthi B. Stereotaxic surgery in cerebral palsy – a study of 57 cases. Neurol India 1970;18(1):56-9. Balasubramaniam V, Kanaka TS, Ramanujam PB. Sterotaxic surgery for cerebral palsy. J Neurosurg 1974;40:577-82. Balasubramaniam V, Kanaka TS, Ramanujam, PB, Ramamurthi B. Stereotaxic hypothalamotomy. Stereotact Funct Neurosurg 1973;35:138-143. Ecker A, Perl T. Percutaneous injection of the thalamus in parkinsonism. Arch Neurol 1960;8:271-8. Varma RM. Percutaneous chemothalamectomy for parkinsonism. Neurol India 1964;12(2):54-60; Varma RM. Percutaneous technique of chemothalamotomy for parkinsonism. Paper presented at third world congress of neurological surgeons, Brussels, 1965. Muthane UB, Varma RM, Sundarajan P, et al. Percutaneous trans-foramen ovale approach to subthalamic nucleus (Varma’s Technique): a shorter route and economical technique in surgical treatment of Parkinson’s disease. Mov Disord 1998;13:71.

39. Muthane UB, Bhatt MH, Wadia NH. Parkinson’s disease and other akinetic disorders. In: Wadia NH, editor. Neurological practice an Indian perspective. Elsevier: Amsterdam; 2005. p. 353-66. 40. Bhagwati SN, Singhal BS. Reactivation of successfully abolished tremors on thalamic stimulation whilst performing surgery for the second side in Parkinson’s disease. Neurol India 1972;20(Suppl 2):166-8. 41. Bhagwati SN. Stereotaxic surgery for Parkinsons’s disease. Bombay Hosp J 1969;2:39-42. 42. Doshi PK, Chhaya NA, Bhatt MH. Bilateral subthalamic nucleus stimulation for Parkinson’s disease. Neurol India 2003;51:43-8. 43. Doshi PK, Chhaya NA, Bhatt MH. Depression leading to attempted suicide following bilateral subthalamic nucleus stimulation for Parkinson’s disease. Mov Disord 2002;17 (5):1084-5. 44. Tir M, Devos D, Blond S, et al. Exhaustive, one-year follow-up of subthalamic nucleus deep brain stimulation in a large, single-center cohort of parkinsonian patients. Neurosurgery 2007;61(2):297-304. 45. Temel Y, Kessels A, Tan S, et al. Behavioural changes after bilateral subthalamic stimulation in advanced Parkinson disease: a systematic review. Parkinsonism Relat Disord 2006;12(5):265-72. 46. Roy TK. Stereotactic cingulate lesions for intractable pain in malignant conditions – a report of 5 cases. Neurol India 1983;31(1):55-8. 47. Ramamurthi B, Davidson A. Progress in stereotactic surgery in Madras. Proc Inst Neurol, Madras 1975;5:81-97. 48. Kalyanaraman S, Ramamurthi B. Studies on the sensory relay nucleus of the thalamus during stereotaxic surgery. Neurol India 1972;20(Suppl 2):155-7. 49. Schaltenbrand G, Bailey P, editors. Introduction of Stereotaxis with an atlas of the human brain. Stuttgart: George Thieme; 1959, p. 2. 50. Kalyanaraman S, Ramamurthi B. Stereotaxic surgery for intractable pain neurology India September 1969;17 (3):109-115. 51. Kalyanaraman S, Logamuthukrishnan S. Stereotaxic posteromedial hypothalamotomy for intractable pain. Proc Inst Neurol Madras 1974;4:95. 52. Govindaswamy MV, Rao B. Bilateral prefontal leucotomy in Indian patients. Lancet 1944;1:466. 53. Anand BK, Brobeck JR. Hypothalamic control of food intake in rats and cats. Yale J Biol Med 1951;24:123-40. 54. Anand BK, Brobeck JR. Loacalization of a feeding center in the hypothalamus of rat. Proc Soc Exp Biol Med 1951;77:323-4. 55. Desiraju T. Fundamental neurophysiology. In: Pandya SK, editor. Neurosciences in India: Retrospect and Prospect, Neurological society of India, 1989, p. 113-52.

History of stereotactic surgery in india

56. Manchanda SK, McBrooks C. Homeo-static controls in the regulation of autonomic nervous system function. In: McBrooks C, Koizumi K, Sato A, editors. Integrative Function of the Autonomic Nervous System. University of Tokyo; 1979. p. 427-430. 57. Kalyanaraman S, Ramamurthi B. Stereotaxic basofrontal tractotomy. Neurol India 1973;21:113-18. 58. Ramamurthi B, Ravi R, Narayanan R. Long term follow-up of functional neurosurgery in psychiatric disorders. experience of 30 cases. The World Conference of Stereotactic and Functional Neurosurgery. Zurich: 1981. 59. Balasubramanium V, Kanaka TS. Stereotaxic surgery of the limbic system in epilepsy. Acta Neurochir 1975;23: 225-34. 60. Balasubramaniam V, Ramanujam PB, Kanaka TS, et al. Stereotaxic surgery for behaviour disorders. In: Hitchcock E, Laitinen L, Vaernet KC, editors. Psychosurgery. Springfield, IL: Charles C. Thomas; 1972. p. 156-63; Ramamurthi B, Ravi R, Narayanan. Functional neurosurgery in psychiatric illness. Indian J Psychiatry 1980;22:261-4. 61. Ramamurthi B, Ravi R, Narayanan. Functional neurosurgery in psychiatric illness. Indian J Psychiatry 1980;22:261-4. 62. Balasubramaniam V. Stereotaxic amygdaloid lesions in behaviour disorders. Ph D. Thesis, Madras University; 1969. 63. Balasubramaniam V, Kanaka TS, Ramanujam PB. Stereotaxic cingulumotomy for drug addiction. Neurol India 1973;21(2):63-6. 64. Balasubramaniam V, Ramamurthi B, Jagannathan K, Kalyanaraman S. Stereotaxic amygdalotomy. Neurol India 1967;15(3):119-22.

12

65. Mayanagi Y, Hori T, Sano K. The posteromedial hypothalamus and pain, behavior, with special reference to endocrinological findings. Appl Neurophysiol 1978;41: 223-31. 66. Arjundas G, Balasubramaniam V, Reddy EC, Ramamurthi B. Hypothalamus and its effects on the viscera. J Assoc Physicians India 1971;19:477-81. 67. Balasubramaniam V, Kanaka TS, Ramanujam PB, Ramamurthi B. Stereotactic hypothalamotomy. Confin Neurologica 1973;35:138-43. 68. Balasubramaniam V, Ramamurthi B, Jagannathan K, Kalyanaraman S. Stereotaxic amygdalotomy. Neurol India 1967;25:119-21. 69. Ramamurthi B. Surgery for aggressive behavior disorders. International Congress Series No 433. Neurological surgery. Proceedings of the Sixth Congress of Neurological Surgery. Sao Paulo; 1977. 70. Gopinath G. Neural transplantation. In: Pandya SK, editor. Neurosciences in India retrospect and prospect. Neurological society of India. 1989. p. 219-30. 71. Mahapatra AK, Gopinath G, Tandon PN. Neural transplantation. Prog Clin Neurosci 1987;1:45-8. 72. Murthy SK, Desiraju T. Quantitative assessment of dendritic branching and spine densities of neurons of hippocampal embryonic tissue transplanted into juvenile neocortex. Dev Brain Res 1989;46:33-46. 73. Muthuswamy R, Sheeladevi A, Namasivayam A, et al. Transplantation of monkey embryonic cortical tissue into the brain of bonet monkey (Macaca radiata). J Anat Soc India 1988;37:27. 74. Muthuswamy R, Sheeladevi A, Namasivayam A, et al. Heterospecific transplantation of human embryonic cortical tissue into the cerebellum of bonnet monkey (Macaca radiata). Neuroscience 1987;22:S765.

169

5 History of Stereotactic Surgery in Japan C. Ohye

Production of the First Stereotactic Instrument and its Application in Human It was post-World War II, when a young bud of stereotactic surgery sprouted in Japan as in other countries. Hirotaro Narabayashi, a postgraduate psychiatrist, inspired by Prof. Ogawa’s suggestion, explored the destroyed and almost burned out Tokyo with a drawing of a stereotactic instrument, looking for a factory that had survived the war. Finally, he found one small factory still working, and with the help of a kind engineer there, he produced the first model of a stereotactic instrument in 1949 [1]. His medical student days during the War were miserable; they were shortened because of heavy air strikes and academic school life almost stopped. In fact, as many Professors and young doctors were summoned for military service, lectures were often cancelled. So Narabayashi spent all his free time in the University Library, where he found an interesting book ‘‘Die Extrapyramidales Erkrankungen’’ by the German pathologist Alfons Jacob [2]. The book proved to be a source of great inspiration and perhaps his idea of using the stereotactic instrument to invade the basal ganglia was born around this time. After graduating from the University of Tokyo in 1945, he joined Professor Uchimura’s Department of Psychiatry in 1946. At that time, there was no separate department of Neurology, so patients with Parkinson’s disease and other involuntary movements were treated in the department of Psychiatryand he noticed that there was no effective treatment for several cases. When Professor #

Springer-Verlag Berlin/Heidelberg 2009

Teizo Ogawa, Professor of Neuroanatomy talked to him about a stereotactic instrument used in animal experiments in Ranson’s Lab in the United States, young Narabayashi was excited and immediately took steps to see if it could be applied to the human brain. However, at that time, with Tokyo almost completely destroyed by bombardment, he had difficulty finding a factory to make such an instrument, as mentioned earlier. Being a passionate young man he had the first stereotactic instrument made in 1949 [3,4]. In 1947, Spiegel and Wycis, Philadelphia, United States, reported the first case of stereotactic surgery on thalamic dorsomedial nucleus for a patient with a neurological problem and movement disorder [5,6]. At that time in Japan, communication with other countries was very limited, and Narabayashi was not aware of the exciting news. Unaware of the work of Spiegel and Wycis, Narabayashi continued to improve on his stereotactic instrument and simultaneously worked on a map of the brain(not published). In 1951, he operated on a patient with cerebral palsy with athetoid movement [1]. But his most exciting success was on June 4, 1952 [7,8], when the first pallidotomy on Parkinson’s disease was successfully completed. After the injection of a small amount of oil wax (procaine-oil and honey wax) the tremors and rigidity disappeared almost immediately and completely. Seeing this miraculous result, Professor Uchimura, chairman of the Department, recognizing the scientific worth in the result encouraged Narabayashi to take this up as his life’s work. Following the Professor’s advice faithfully Narbayashi devoted his whole life to this field of stereotaxy. There

60

5

History of stereotactic surgery in Japan

is a moving anecdote reported in the story of his first pallidotomy. The patient was a relatively young telecommunist suffering from tremors and rigidity. The patient was a very generous man and agreed to undergo the new brain operation without any guarantee. The first and the second operations to caudate nucleus and putamen were in vain. When Narabayashi pleaded for a third attempt, the patient willingly accepted and Narabayashi’s enthusiasm was rewarded with triumph. Another important and unforgettable episode that centered around his first pallidotomy was, the now well known but controversial at that time, the bitter criticism of Spiegel and Wycis and the firm response from Narabayashi. However, Spiegel and Wycis soon recognized the hardwork of Narabayashi and a deep understanding of each other’s scientific attitude fostered a long lasting friendship between them. The letters they exchanged were published in the Archives of Neurology and Psychiatry in 1956 and were later reproduced in a tribute to Narabayashi [9,10]. For several years after the war, the Japanese people had a very difficult time with shortage of food, bare necessities, housing etc. Nevertheless, the Japanese people worked hard, doctors with poor medical facilities were no exception. In the Japanese University Clinic, Neurosurgery including stereotactic surgery was started in earnest. Stereotactic surgery attracted many young neurosrgeons and as a natural consequence Narabayashi became the central figure. He extended his stereotactic research working with young researchers of the Brain Research Institute, University of Tokyo, where Professor Toshihiko Tokizane chaired the Neurophysiology section. Narabayashi recognized from the very beginning, that cooperation with researchers in the basic sciences was essential for the development of stereotactic surgery; the author is one of those who worked with him. In 1956 he moved to Juntendo University as Associate Professor of Psychiatry, but in 1957 he founded his own private clinic devoted mainly to

stereotactic surgery; this became a world famous ‘‘Neurological Clinic’’ later on. As Narabayashi was very frank and open minded, many young doctors gathered in his clinic to see new operations and discuss freely with him. His clinic became a salon for discussions on not only stereotactic surgery, but all areas of Neuroscience. From this salon, in fact, many fledgling doctors of Neuroscience – neurologists, neurosurgeons, neurophysiologists, neurochemists, neuroanatomists etc. – have emerged as leaders in their fields. Narabayashi’s contribution in this sphere also has been remarkable.

Birth of the Japanese Society of Functional and Stereotactic Surgery Many Professors of Neurosurgery [11–13] gathered around Narabayashi, and the Japanese Society for Research in Stereoencephalotomy was founded in 1963, following the International Society, which was founded in 1961 The first Meeting was held in Kyoto, February, 1963, hosted by Professor Araki of Kyoto University. The second Meeting was held in June of the same year organized by Professor Takebayashi of Wakayama Medical School. After the third meeting in the following year, the Japanese Society has been meeting regularly every year, so the 47th Meeting will be held in 2008, organized by Professor Namba of Hamamatsu Medical School. We are very proud that the annual meetings have been conducted regularly without interruption. At one point of time there was an effort to establish the Japanese Society (a research group) but the research fund provided by the Japanese Ministry of Education for the purpose of ‘‘Stereotaxic deep brain surgery’’ was accepted by our Society. This governmental support was, in fact, the successor to the previous research fund for the ‘‘Study on the extrapyramidal movement disorder.’’ The name of the society was changed, following the name of the World Society to

History of stereotactic surgery in Japan

‘‘the Japanese Society for Stereotactic and Functional Neurosurgery’’ in 1973. At the first meeting, some 50 interested doctors came from several centers and 13 papers from different University clinics were presented including my special lecture on neurophysiology of the basal ganglia symptoms. There were many lively discussions on this new operation. At present the society has 500 odd members and some 100 papers were presented during the two days of the meeting with lively discussions. We pride ourselves on the organization of these meetings and the free and active discussions. Narabayashi attended the first International Meeting of Neurology and Neurosurgery in Brussels in 1959. In the stereotactic section he was the first Japanese to attend an international meeting. He presented his work on pallidotomy, met most of the pioneering stereotactic surgeons from all over the world who shared their initial experiences of stereotactic surgery. Narabayashi’s work on pallidotomy was appreciated by many. It was very important that the Japanese development of stereotaxy was recognized even in the early stages. Sterotactic surgery was once prevalent all over Japan.Asin othercountries almost every Neurosurgical Department has a stereotactic unit. Following are the names the first generation of stereotactic surgeons in Japan with their areas of work: Ueki (Niigata) – Ultrasonic device, Sano (Tokyo) – hypothalamotomy for behavior disorder, Narabayashi,Nagao(Tokyo)–pallidotomy,Takebayashi, Komai (Wakayama) – Superior colliculus for Nystagmus, Araki, Handa (Kyoto) – Torticollis, Ozawa, Hori (Osaka) – Epilepsy, Jinnai, Nishimoto (Okayama) – Forel H, Hoshino (Hiroshima) – Radioisotope. Many young stereotactic neurosurgeons went abroad (USA, Canada, Germany, France, Swiss, Sweden, Italy, England etc.), to learn about the different aspects of stereotactic surgery. Sterotactic surgery has progressed rapidly in Japan and consequently, nowadays, several young stereotactic doctors of second and third generation attend

5

international meetings related to modern stereotactic research and treatment in the United States and in Europe.

The Ups and Downs of the Society Around the 1970s stereotactic surgery went through several ups and downs. One of the unhappy incidents was the world wide student violence toward the end of the 1960s, known as the Zengakuren in Japan. Some professors were attacked by the students, professors of Psychosurgery being their main focus. Unfortunately the hypothalamotomy of Sano and the amygdalotomy of Narabayashi had to be stopped. As a consequence, the stereotactic team in Tokyo University was almost disbanded, which resulted in a great loss for the progress of stereotactic surgery in Japan. Another critical event for the world of stereotactic surgery was the progress in the L-dopa drug therapy for Parkinson’s disease around the 1970s that sidelined the surgical option. The next 20 years were difficult times for stereotactic surgeons all over the world [14]. In Japan the surgeries were reduced and many Neurosurgical Departments closed their stereotactic section. But Narabayashi’s group continued with surgeries because of his reputation, and the microrecording technique learnt from the French group (Albe-Fessard and Guiot) by Ohye was established during this time. Thereafter, microrecording during stereotactic surgery became one of the prestigious features in Japan. It also gave us an opportunity to study the functional organization of the human thalamus (see ‘‘Thalamotomy’’ in this book). On the other hand, the use of L-Dopa for more than 10 years brought to light an unexpected new hazard in the treatment of Parkinson’s disease. As every one is aware, L-Dopa is quite effective for a few years initially but it has complicated side effects. This inevitably suggests revival of the surgical treatment.

61

62

5

History of stereotactic surgery in Japan

Nevertheless, during this period, the Japanese Society continued to have its annual meetings as before. One aspect of the scientific activity of the Japanese Society, the number of presentations in each year’s meeting, is shown in > Figure 5-1 [15]. It is clear from the figure that the number of papers presented at these meetings has grown steadily from 20 papers in the earlier years to nearly 100 papers in recent times. As a result of this increase, since the 39th meeting (in Fukuoka, in 2000), the Society meets for two days. In addition, the Society, which usually held its meetings just before the Annual Meeting of the Japanese Society of Neurosurgery (usually one day earlier), has since the 43rd meeting in Nara become independent of the general neurosurgery meeting. Moreover we have two local functional neurosurgery study groups namely, the Kanto (East Japan) Functional Neurosurgeon Conference twice a year and the Yamaguchi and Kyusyu

(Western) Stereotactic Neurosurgery Seminar once a year. The former had its 25th conference in 2007, and the latter its 15th seminar in 2007. In effect, our Japanese stereotactic group continues to be very active.

New Age of Stereotactic Surgery During the ‘‘cold age’’ of stereotactic surgery, we had a few pleasant events. Narabayashi hosted the World Society Meeting in Tokyo in 1973, and Ohye the 10th Meeting in Maebashi in 1989. They both served as the President of the World Society following each World Society Meeting they hosted. Further, Narabayashi was awarded the Spiegel Wycis Medal, the highest honor of the Society, in 1989, and Ohye received it in 2001. The Japanese Society is very proud of them. The Japanese Society continued its activity into the new age. We now have several advanced

. Figure 5-1 Time sequential change of number of papers (ordinate) presented at the Annual Meeting of Japanese Society from the beginning (1st) to the present time (47th) (Abscissa). Results of 21st–35th meeting were omitted. Note that since 39th meeting, we had two days meeting, and the submitted pages increased from the next year of 2001. The 15th meeting was somewhat different from others. It was invited lectures by foreign guests and related discussions

History of stereotactic surgery in Japan

techniques in surgery and fresh knowledge of the basal ganglia and hence, Parkinson’s disease. Computerized imaging system is now close to neurosurgeon’s hand to visualize deep brain structures in 3D fashion. Understanding Parkinson’s disease opens several new avenues that are still growing. On the other hand, advanced new surgical technology has given us new tools – chronic stimulation by implanted electrode initiated by A. Benabid in France, stereotactic radiosurgery using Gamma knife by L. Leksell, brain graft and etc. We are now in a new era of stereotaxy with many new possibilities. In fact, more than ten stereotactic centers are actively involved in stereotactic selective thalamotomy with microrecording, chronic stimulation of different targets including the thalamus, GPi, subthalamic nucleus, or stimulation of cerebral cortex (initiated by Tsubokawa), Although we do not yet know the optimal target for the treatment of different symptoms, we are quite optimistic about the future of stereotactic surgery, because the idea of stereotaxy is now widely applied in the field of general neurosurgery and therefore it stands at the center of Neurosurgery. Without stereotaxy, precise minimally invasive neurosurgery cannot be performed.

References 1. Kanazawa I. Interview with Professor Narabayashi. Tracing the idea and footstep of a neurologist. Prog Neurol 2001;45(3):512-22 (Japanese).

5

2. Jacob A. Die extrapyranuidale Erkrankungen. Berlin: Springer-Verlag; 1923. 3. Narabayashi H. (Stereotaxic apparatus (Model II) (Japanese). Psychiat Neurol Jpn 1953;54:669. 4. Uchimura Y, Narabayashi H. Stereotaxic apparatus. Psychiat et neurol 1951;52:265-70. 5. Spiegel EA, Wycis HT. Pallido-thalamotomy in Chorea. Arch Neurol Psychiat 1950;64:495-6. 6. Spiegel EA, Wycis HT, Marks M, Lee AJ. Stereotaxic apparatus for operations on the human brain. Science 1947;106:349-50. 7. Narabayashi H, Okuma R. Procaine oil blocking of the globus pallidus for the treatment of rigidity and tremor of parkinsonism (priminary report). Proc Jpn Acad 1953;29:134-7. 8. Narabayashi H, Okuma T, Shikiba S. Procaine oil blocking the globus pallidus. Arch Neurol Psychiatry 1956;75:36-48. 9. Ohye C, Fodstad H. Forty years with professor Narabayashi. Neurosrgery 2004;55:222-7. 10. Spiegel EA, Wycis HT. Procaine oil blocking the globus pallidus (letter). Arch Neurol Psychiatry 1956;76:263. 11. Narabayashi H. Stereo encephalotomy in Japan. Conf Neurol 1964;24:314-20. 12. Narabayashi H. Begging and development of sterotaxic surgery in Tokyo. Conf Neurol 1975;37:364-73. 13. Ohye C, Fodstad H. Prof. Hiro Narabayashi: in memoriam. Stereotact Funct Neurosurg 2001;76:125-8. 14. Ohye C. Stereotactic surgery of Parkinson’s disease over 30 years. In: Mizuno Y, Fisher A, Hanin I, editors. Mapping the progress of Alzeimer’s and Parkinson’s disease. New York: Kluwer Academic/Plenum Publishers, (2002) p. 429-34. 15. Matumoto K., Abstracts of the papers presented at the 1st–20th meeting of the Japanese society of stereotactic and functional neurosurgery. Neuron Tokushima, Tokyo; 1892.

63

13 History of Stereotactic Surgery in Korea S. S. Chung

In Korean history, the end of the nineteenth century is considered as the period of the Chosun Dynasty’s transition from medieval to modern. This period was marked by wide-ranging social and economic changes on the domestic front, and, externally, by the threat of foreign domination. It was during this period when modern medicine began, perhaps personified historically when Dr. Horace N. Allen (> Figure 13‐1), a Protestant missionary from the Presbyterian Missions in New York, stepped onto Korean soil. In December 1884, Allen was given the opportunity of saving the life of Queen Min’s nephew. In gratitude, at the behest of King Kojong, the Royal Hospital Kwanghyewon, ‘‘House of Extended Grace,’’ was founded on 10 April 1885, and on April 23rd the name was changed to Chejungwon (> Figure 13‐2), which means ‘‘Universal Helpfulness,’’ Kwanghyewon was the first modern hospital in Korea, which later became the Severance Hospital, an affiliate of the Yonsei University Medical School [1,2]. The hospital provided a legitimate venue for the first protestant missionaries to pursue their religious activities while conducting systematic research on diseases endemic to Korea. In March 1886, a year after the founding of Chejungwon, the hospital launched its Medical Department to educate future medical practitioners and professionals in modern medicine, aiming to treat the ailments of the Korean people. Since Allen had been appointed as head of the hospital, J. E. Heron, Charles C. Vinton, and Oliver R. Avison (> Figure 13‐3) successfully carried on his work as a director of the hospital. #

Springer-Verlag Berlin/Heidelberg 2009

As the result of advances made possible by Avison’s fund-raising initiatives in the United States, in 1899 the Medical Department of Chejungwon was accredited as a full-fledged medical educational institution. An American entrepreneur, Louis H. Severance, deeply moved by Avison’s speech about his missionary activities in Chosun, decided to donate $10,000, a very large sum of money in 1900. With funding provided by Severance, a new hospital building was completed on 23 September 1904. It was named Severance Hospital (> Figure 13‐4) to commemorate the man who had made it possible. It was Korea’s first modern Western style hospital building. In 1908, the Chejungwon Medical School (later Yonsei University Medical School) celebrated its first graduation. While the Chejungwon Medical School was founded and established, several medical schools were also founded in sequence. In the early 1940s, a few pioneering general surgeons started to practice neurosurgical procedures in medical school accredited hospitals. The neurosurgical procedures included neurotraumas, epilepsy surgeries, and surgeries for mental disorders. Actually all the early stage neurosurgeons were functional neurosurgeons. In 1943, Dr. Chu Kul Lee performed corticectomy on a patient with posttraumatic epilepsy. Dr. Lee graduated from Daegu Medical College (later Kyungbook National University) in 1937 and continued to study neurosurgery in Nagoya University, Japan. He returned to Korea in 1942 and proceeded to perform cortical resection for epilepsy patients in Seoul’s Women’s Medical College (later Korea University Medical College).

172

13

History of stereotactic surgery in korea

Later on he conducted cortical coagulation to interrupt the epileptic impulse in patients with epilepsy. He was interested in epilepsy surgery throughout his neurosurgical career and . Figure 13‐1 Dr. Horace N. Allen; Presbyterian missionary from New York who founded the first Western style hospital, Chejungwon on 10 April 1885

published his experience in the first issue of the official Journal of the Korean Neurosurgical Society in 1972 [3]. He was a leading figure in the neurosurgical field and trained many neurosurgeons in 1960s. He was elected as the first president of the Korean Neurosurgical Society in 1961. Another pioneer was Dr. Ki Sup Lee. He graduated from Severance Medical College (later Yonsei University) and studied neurosurgery in Kyoto University, Japan. He performed frontal lobotomy for mental disorder, corticectomy for epilepsy, and sympathectomy for pain in Severance hospital in 1943 (Lee KS, 1996, personal communication). Dr. Si Chang Kim graduated from Kyungsung University (later Seoul National University) in 1936. At one stage, he worked in Seoul Women’s Medical College and returned to Kyungsung University Hospital in 1948 where he performed corticectomy and cortical vessel ligation for epilepsy sufferers. He was one of the handful number of active surgeons practicing neurosurgery at that time. Unfortunately, he was

. Figure 13‐2 Chejungwon in Seoul (1885); the first Western style hospital in Korea

History of stereotactic surgery in korea

abducted and taken to North Korea during the Korean War (Moon TJ, Forty years History of the Korean Neurosurgical Society (19612001), 2002, personal communication).

. Figure 13‐3 Oliver R. Avison (served 1893–1935); Canadian missionary who was director of Chejungwon hospital and later Dean of Severance Medical College

13

The Korean War broke out on the 25 June 1950. War-related trauma injuries provided great momentum to the development of neurosurgery in Korea. During the Korean War, Scandinavian countries sent the Danish hospital ship Jutlandia to Busan to care of casualties. The chief neurosurgeon on this ship was Professor Edward A. V. Busch from Copenhagen University, Denmark, and his assistant was Dr. K. Vaernet. They not only treated patients but also taught neurology and neurosurgery to Korean military surgeons. Many American military surgeons also came to Korea during the war, among them colonel Arnold M. Meirowsky and George J. Hayes contributed enormously to the development of neurosurgery in Korea. They served in the mobile army surgical hospitals (MASH) and also taught neurosurgery to Korean military surgeons [4]. Some Korean surgeons had several months of continuous neurosurgical training, which served them well in organizing neurosurgical teams. Casualties from the war included patients with cranio-spinal trauma, peripheral nerve injury, and causalgia. The neurosurgeons in the army

. Figure 13‐4 Severance Hospital (1904), the first Western style hospital building in Korea. Louis H. Severance, businessman from Cleveland, donated for the new hospital building and Chejungwon Hospital was renamed as Severance Hospital

173

174

13

History of stereotactic surgery in korea

performed many thoracic sympathectomy for patients with causalgia. It was a great opportunity for the Korean neurosurgeons to observe Western medicine and neurosurgical practices. After the war some of them continued to practice neurosurgery while others went abroad to study neurosurgery in Western countries [4]. In the late 1950s, neurosurgeons who went abroad came back to Korea after completing neurosurgical training. Dr. Tae Joon Moon had residency training at Thomas Jefferson University (USA), and became a qualified neurosurgeon by the time he came back in 1957. Upon his return, he practiced neurosurgery in Yonsei University and performed trigeminal ganglion block with hot saline or absolute alcohol in the treatment of trigeminal neuralgia and open thoracic cordotomy for intractable cancer pain. Dr. Bo Sung Sim graduated from Seoul National University in 1949. He served as an army neurosurgeon during the Korean War and studied neurosurgery in Minnesota University (USA). He performed hemispherectomy in patients with intractable epilepsy due to cerebral paragonimiasis in 1958. He also performed retrogasserian rhizotomy in the middle cranial fossa for trigeminal neuralgia [4]. Dr. Hun Jae Lee graduated from Severance Medical College in 1944 and finished his residency program in Michigan University Hospital (USA) to become a qualified neurosurgeon. He came to Seoul Women’s Medical College in 1959, after which he performed open cordotomy for intractable cancer pain and retrogasserian rhizotomy for trigeminal neuralgia, while also applying alcohol in gasserian ganglion percutaneously for trigeminal neuralgia [5]. Dr. Kon Huh graduated from Severance Medical College in 1948, and continued studying neurosurgery in Wisconsin University (USA). He came back to Severance Medical College in 1962 where he practiced pain surgery such as open cordotomy or retrogasserian rhizotomy in middle cranial fossa [4]. Dr. Jeong Wha Chu graduated from

Seoul National University in 1956, and studied neurosurgery in Minnesota University (USA). After coming back from Minnesota University in 1961, he practiced some ablative pain surgeries such as open cordotomy and retrogasserian rhizotomy in middle cranial fossa [6]. Stereotactic surgery in Korea began in the early 1960s. Dr. Hun Jae Lee performed chemothalamotomy in patients with Parkinson’s disease using Cooper’s frame in 1960. It was the first stereotactic surgery using stereotactic apparatus in Korea. He presented the results of chemothalamotomy in seven cases of Parkinson’s disease patients and four cases of dystonia patients. He reported on follow up results of those patients in 1963 (Chu JW, 2006, personal communication). Dr. Tae Joon Moon also performed thalamotomy using simple burr hole mounted Mackinie apparatus. Dr. Chul Woo Lee of Kyungbook University, who trained at the Saint Vincent Hospital in Wooster city near Boston (USA), made his own stereotactic frame in 1960. He performed thalamotomy for patients with dystonia and Parkinson’s disease. Dr. Jeong Wha Chu also performed thalamotomy for patients with Parkinson’s disease [6]. However, there were very few neurosurgeons who carried out stereotactic surgery for movement disorders at that time. In 1971, the radiofrequency lesion generator was introduced in to Korea. Sang Sup Chung of Yonsei University performed percutaneous radiofrequency cervical cordotomy, radiofrequency trigeminal thermocoagulation, and radiofrequency ventrolateral thalamotomy for Parkinson’s disease sufferers in 1972 [7,8]. In 1973, radiofrequency facial nerve neurotomy was performed for hemifacial spasm at the stylomastoid foramen [9]. It was the beginning of the subspecialty of stereotactic and functional neurosurgery in Korea. Introduction of radiofrequency lesion generator made it possible for many procedures to be conducted percutaneously, allowing for a more accurate,

History of stereotactic surgery in korea

safer, and simpler operation. In 1976, Computed tomography (CT) scanner was introduced in to Korea. The introduction of radiofrequency lesion generator and CT scanners were substantial moments for the development of stereotactic and functional neurosurgery in Korea. In 1975, Sang Sup Chung went to Edinburgh University, Britain, for further study where he practiced stereotactic and functional neurosurgery under professors F. John Gillingham and Edward R. Hitchcock. After returning to Yonsei University he became a fulltime stereotactic and functional neurosurgeon. In 1976, Chang Rak Choi studied functional neurosurgery under professor Umbach in Berlin, Germany, and came back to Catholic University where he continued to practice stereotactic and functional neurosurgery. In 1978, Dr. Kil Soo Choi and Dr. Hun Jae Lee performed microvascular decompression for hemifacial spasm and trigeminal neuralgia. Soon after, Sang Sung Chung followed the procedures [10]. In 1979, depth recording was performed using semi-micro electrode during thalamotomy. In the 1980s there was rapid progress in research activities and surgical techniques in Korea. Various stereotactic and functional surgeries were performed. In 1980, Sang Sup Chung performed stereotactic chemical or radiofrequency hypophysectomy [11], percutaneous spinal rhizotomy and percutaneous medullary trigeminal tractotomy in treating cancer pain. Dorsal root entry zone lesioning and facet denervation were performed for chronic intractable pain and for chronic low back pain. Centrum medianum and parafacicularis nucleus lesioning were done for chronic central pain. Hypothalamotomy was performed for aggressive psychosis and glycerol injection was introduced as a treatment modality for trigeminal neuralgia. Also in 1980, percutaneous spinal cord stimulation for chronic pain and intrathecal infusion pump were introduced for cancer pain. However, these devices were not covered by insurances and it was difficult to treat many patients in the early stages of diagnosis

13

because of economic problems. During this period, various newly developed functional neurosurgical procedures were attempted while a number of stereotactic apparatus such as ToddWells, Riechert-Mundinger, Guiot-Gillingham, BRW frame were introduced in to Korea. In the 1980s, CT compatible CRW, Hitchcock, and Leksell frame, which were introduced, enabled surgeons to perform image guided surgery. In 1984, stereotactic evacuation of intracerebral hematoma or brain biopsy was carried out by CT image guided surgery. In 1982, Moon Chan Kim came back to Catholic Medical College after studying in Birmingham under Professor Hitchcock. As a full time neurosurgeon, he practiced surgery for movement disorder, pain, and psychiatric illness. In 1988, linear accelerated based radiosurgery were performed by Moon Chan Kim and Sang Sup Chung. In 1988, Sang Sup Chung performed adrenal gland transplantation for Parkinson’s disease sufferers and reported on the 5 year follow-up results in 1993 [12]. Epilepsy surgery was conducted sporadically from its inception. However, a comprehensive epilepsy protocol (Yonsei Epilepsy Protocol) was established in 1989, after which epilepsy surgery became more standardized and several centers were built. During the 1990s, stereotactic and functional neurosurgery achieved substantial development owing to the great technological advancements in computer science, surgical softwares, engineering, neurophysiology, and various diagnostic tools. The resolution of MRI improved immensely and accurate MRI guided surgery became possible from 1995. In 1999, vagal nerve stimulation was done for intractable epilepsy and microdepth recording started during thalamotomy. Deep brain stimulation for Parkinson’s disease was introduced in 2000 by Jin Woo Chang and Sang Sup Chung. From late 1980s through to the 1990s, many young neurosurgeons were getting interested

175

176

13

History of stereotactic surgery in korea

in stereotactic and functional neurosurgery. Uhn Lee of Ghil Hospital, who graduated from Hanyang University, is an active neurosurgeon who treats patients with movement disorders. He conducted thalamotomy and pallidotomy in the late 1980s and now continues to practice DBS. Jae Hyoo Kim of Chonnam University is also an active functional neurosurgeon, who is carrying out pain surgery, DBS for movement disorders and sympathectomy for hyperhidrosis. Jin Woo Chang graduated from Yonsei University and studied at the University of Chicago (USA). He is also an active functional neurosurgeon doing DBS surgery for movement disorders, pain surgery and psychosurgery. Others are Sung Nam Hwang of Chungang University, Young Soo Kim of Hanyang University, Yong Tae Chung of Busan Baik Hospital, Kyung Jin Lee of Catholic University, Jung Yul Park of Korea University, Seong

Ho Kim of Yeungnam University, Young Hwan Ahn of Ajou University, Jeong Il Lee of Samsung Medical Center, Moo Seong Kim of Busan Baik Hospital and Ryoong Huh of Pochon Cha University. They are all active in the treatment of movement disorders or pain surgery. The Korean stereotactic and functional neurosurgery society was founded on February 24th 1990, and the first president and secretary were Sang Sup Chung and Chang Rok Choi, respectively (> Figure 13‐5). Approximately 150 members were registered with the society in 2006. In 1996, Sang Sup Chung was elected as the president of the Asian Society of Stereotactic, Functional and Computer assisted Neurosurgery. In 1999, he held the third Asian Society meeting in Seoul successfully (> Figure 13‐6). The first Gamma Knife unit was installed in 1990, and now there are 11 gamma knife units

. Figure 13‐5 The first meeting of the Korean Sterotactic and Functional Neurosurgery Society; Seoul, February 24, 1990

History of stereotactic surgery in korea

13

. Figure 13‐6 The third meeting of Asian Society of Sterotactic, Functional and Computer assisted Neurosurgery; Seoul, June 13, 1999

in Korea. In 2006, 2700 gamma knife radiosurgeries were conducted in Korea. The gamma knife radiosurgery society meeting was held on 15th of November 2002 and there have been also annual meetings thereafter. The neurosurgeons involved in radiosurgery are Yong Gou Park of Yonsei University, Dong Gyu Kim of Seoul National University, Young Jin Lim of Kyunghee University, Do Hoon Kwon of Seoul Asan Hospital, and Chang Wha Choi of Busan National University. In 2006, Dong Gyu Kim organized the 13th international meeting of Leksell gammma knife society in Seoul successfully. In the beginning of functional neurosurgery, our pioneers conducted epilepsy surgery, while epilepsy surgery according to a comprehensive proocol began in 1989. The Korean epilepsy

society was founded in 1996 and Sang Sup Chung was elected as the first president. Many active and functional neurosurgeons are participating members of the epilepsy society. Active epilepsy surgeons are Jung Kyo Lee of Seoul Asan Hospital of Ulsan University, Hyung IL Kim of Chunju Presbyterian Hospital, Eun Ik Son of Kyemyung University, Seung Chyul Hong of Samsung Hospital, Chun Kee Chung of Seoul National University, Ha Young Choi of Chonbuk National University and Jong Hee Chang of Yonsei University. Many of the institutes use Leksell stereotactic apparatus while 54 hospitals have Leksell apparatus. Many of the hospitals are using the apparatus simply to conduct brain biopsy or evacuation of hematoma. Nineteen hospitals performed 271 DBSs in 2006; 190 Parkinson’s

177

178

13

History of stereotactic surgery in korea

disease, 34 Essential tremors & 36 Dystonia. There were also clinical experiment of DBS for epilepsy and psychiatric disorders. With more than 60 years of achievement, stereotactic and functional neurosurgery has evolved and become one of important fields of neurosurgery in Korea.

References 1. Commemorating symposium of 122nd anniversary of Chejungwon. Evolution of modern medicine in Korea. Yonsei University Medical Center. 2007. 2. Photographs of 120 years of modern medicine in Korea. Yonsei University Medical Center. 2007. 3. Lee CK. Surgical Treatment of Epilepsy, Preoccipital Coagulation. J Kor Neurosurg. 1972;1:1-14. 4. Forty years History of the Korean Neurosurgical Society (1961~2001). The Korean Neurosurgical Society. 2002. 5. Woo CH, Chang NS. Anterolateral Cordotomy for Relief of Various Intractable Pain. Kor J Soci. 1963;5:121-5.

6. Woo CH. Stereoencephalotomy for Extra Pyramidal System Disorders. J Kor Medi Assoc. 1963;6:248-58. 7. Lee CW. A new method of stereotactic Encephalotomy for Dystonia and Dyskinesia. Modern Med. 1960;3:69-78. 8. Chung SS, Park TS, Kim CS, et al. Percutaneous radiofrequency rhizotomy for Trigeminal neuralgia. J Kor Neurosurg. 1975;4:323-9. 9. Kim SH, Lee KH, Chung SS, et al. Percutaneous cervical radiofrequency Cordotomy for Intractable pain. Yonsei Med J 1975;16:72-82. 10. Doh JW, Park JU, Chung SS, et al. Percutaneous Neurotomy for Clonic Facial Spasm, a case report. J Kor Neurosurg. 1975;4:331-4. 11. Kim SH, Chung SS, Lee HJ, et al. Neurovascular decompression in posterior fossa for Trigeminal Neuralgia. J Kor Neurosurg. 1981;10:469-75. 12. Chung SS, Lee HJ, Lee Ks, et al. Stereotatic radiofrequency hypophysectomy, for disseminated breast and prostate cancer: Transseptal trans sphenoidal approach. Yonsei Med J. 1981;22:53-7. 13. Chung SS, Park YG, Chang JW, Cho J. Long term follow-up results of Stereotactic adrenal medullary transplantation in Parkinson’s diseases. Stereotact Funct Neurosurg. 1994;62:141-7.

14 History of Stereotactic Surgery in Spain J. Guridi . M. Manrique

The history of stereotaxy in Spain dates back to the mid-1950s. Its early history was constrained by the negative impact of the Spanish Civil War on the development of medicine, as on other areas of Spanish society. However, during the 1960s, when various neurosurgeons returned to Spain, the speciality grew. Today it is difficult to find reports of surgical interventions performed by neurosurgeons during that time; in some cases, oral transmission provided the only way of finding out about the development of functional stereotactic surgery in Spain during the 1950s and 1960s. Historical concepts concerning movement disorders developed during the early years of the twentieth century. As a result of early pathological studies on Huntington’s or Wilson’s disease, encephalitis letargica and Parkinson’s disease (PD), which affected subcortical circuits such as the striatum, pallidum, subthalamic nucleus (STN), and substantia nigra, it was discovered that the basal ganglia were involved in motor function. The understanding of the extrapyramidal motor system and movement disorders constituted a turning point in the neurosurgical field. Meyers operated on a patient with postencephalitic parkinsonism in 1939, resecting two-thirds of the caudate head using a transcortical-transventricular approach, and achieving complete arrest of tremor [1]. This pioneering procedure was followed by other operations approaching the caudate nucleus, internal capsula and globus pallidus (GP) with the ansa lenticularis. At that time, the GP was the target of choice for PD and for hyperkinetic disorders; early surgery was performed by open #

Springer-Verlag Berlin/Heidelberg 2009

procedures, and later with the stereotactic armamentarium. The first stereotactic operation in humans was performed in 1947 by Spiegel (a neurologist) and Wycis (a neurosurgeon) in Philadelphia, on a patient with a psychiatric disorder. They called stereoencephalotome to the first frame, and an account of this significant technical advance and its benefits for patients was published in Science [2]. During the first decades of the twentieth century, general surgeons performed brain operations in different hospitals in Spain. Initially, some of them were in close contact, and worked under the direction of a neurologist, because early neurosurgery was not well developed in the country. After the Spanish Civil War (1936–1939) and the Second World War (1939– 1945), the creation of the National Health System facilitated the development of specialties, which contributed to medical advances in the field of the neurosurgery in the 1950s. Dr Obrador was a pioneering neurosurgeon, who spearheaded and worked in specific areas in the field of surgical neurology. On one of their several visits to different neurosurgical departments, Obrador went to Oxford with Sherrington, where Liddel was using stereotactic methods in monkeys. Later, he visited Dr. Fulton in New Haven and Bailey in Chicago, where he came to know and study techniques relating to the implantation of electrodes producing localized deep cerebral lesions. The first Spanish experience in the functional field was with electrostimulation and the coagulation of the thalamus in a patient with localized myoclonic epilepsy and in whom a previous cortical excision had failed [3].

180

14

History of stereotactic surgery in Spain

1955–60 Dr Obrador performed GP lesions in parkinsonian patients in 1955; he described a simplified and open technique, approaching the pallidal region from a temporal burr hole and performing a mechanical lesion with a pallidotome without stereotactic armamentarium [4,5]. The instrument described was a canula with a wire loop at the lower end; the rotation of the instrument (the loop) severs the tissue. However, the wire loop may tear tissue and blood vessels resulting in an irregular and non-predictable lesion. Obrador, along with Dierssen, wrote a groundbreaking report describing 100 lesions, (95 in the pallidum and 5 in the thalamus) in 69 patients (55 parkinsonian and 14 hyperkinetic) [6]. The authors reported that 67 surgical procedures had been carried out, involving mechanical lesions. Nine lesions were placed using the mechanical-chemical procedure; five were made using the Cooper balloon technique; a further nine chemical lesions, with alcohol; and ten through stereotactic electrocoagulation. The results showed that, whatever the surgical technique used, more than half of the lesions (56%) led to a dramatic alleviation of rigidity, tremor and general patient mobility [6]. However, during the follow-up period, from months to 3 years, clinical signs returned in a high percentage of cases. The report’s authors concluded that only 32% of the parkinsonian patients who received surgical treatment could be regarded as improved after that time. The complications arising after open surgical procedures were also detailed: facial paresis appeared in 20 of the 79 lesions; 17 patients showed contralateral hemiparesia; there were speech disorders in 7 cases; and cognitive changes in 8 patients. One patient died after mechanical pallidotomy [6]. This interesting report on early neurosurgery in Spain showed a high degree of failure in the clinical signs of parkinsonian patients in lengthy follow-up periods, along with a high

percentage of complications caused by the open surgical procedure. Consequently, the open approach to deep structures such as basal ganglia without stereotactic apparatus was practically abandoned, because it had become obvious that lesion placement was only well controlled using stereotactic armamentarium. There was no stereotactic frame in the country at that time; thus, a number of Spanish neurosurgeons went abroad to learn how to use different stereotactic instruments. In those days, Irving Cooper was a renowned and charismatic neurosurgeon working in the field of movement disorders and, in particular, PD. G Bravo (1957–60), G Dierssen (1958–61) and F Isamat (1960–61) – all from Spain – worked with him at St Barnabas Hospital in New York. This period encompasses a significant moment in the history of neurosurgery, when the surgical target in parkinsonian patients was shifting from the pallidum to the ventrolateral (VL) of the thalamus. At St Barnabas, Cooper and Bravo developed a technique for lesioning in the GP and thalamus. They introduced a balloon on the target, inflating it with air or a liquid and inserting it into the lumen as a compressive test. If the patient improved, the lesion was later produced with alcohol [7–10]. On the basis of this early technique, in conjunction with chemopallidectomy or chemothalamectomy, rigidity was alleviated by 80% and tremor by 75% in parkinsonian candidates after a 4-year follow-up period [9,10]. Cooper and Bravo showed that if the lesion was performed accurately on the target, the improvement induced as a result held for a long follow-up period. Their surgical procedure produced some adverse effects, such as a mortality of 2.4% and 2% hemiplegia in patients treated [9]. Alcohol injections in the brain’s deep structures also had irregular diffusion in the tissue, lesioning cellular and fiber elements without affecting vessels. Cooper et al reintroduced alcohol through the chemopallidectomy approach,

History of stereotactic surgery in Spain

preparing a mixture of ethyl cellulose and ethanol (etopalin) to prevent diffusion in the target. They reported, as Hassler had in Germany, that the interruption of fibers between GP and thalamus was very important for clinical alleviation in parkinsonian and hyperkinetic disorders [10,11]. The lesions in the GP provided good relief of rigidity but less consistent improvement of tremor [10]; they later reported that the alleviation of tremor and rigidity in parkinsonian patients was obtained after a lesion was placed in the VL of the thalamus. Dr Cooper and Bravo made a striking discovery. Cooper planned to perform a lesion in the posterior part of the GP (15 mm behind Monro foramen) in a tremoric patient; after surgery, the tremor disappeared. However, the patient committed suicide 6 months after surgery, and the brain was analyzed in the hospital. The autopsy, which was carried out by Bravo, revealed that the lesion was placed in the VL of the thalamus. Based on this information, Cooper and Bravo changed the surgical approach from the GP to the VL of the thalamus as “the most effective lesion for producing complete and enduring relief of parkinsonian tremor and rigidity” [7,8]. The surgical results with the GP lesion (pallidotomy) for the alleviation of rigidity and tremor in parkinsonian patients were disappointing because large lesions had to be made in the nucleus if improvement was to be obtained. This prompted Hassler to study the pallidal projections to the thalamus; he showed that most of the pallidal efferences projected in the ventral lateral nuclear region: in his own classification, ventralis oralis anterior (Voa). As a consequence, he proposed performing a lesion on the new target; nevertheless, despite the shift to the thalamus, the surgery did not effect total abolition of parkinsonian tremor [11,12]. Whether the shift was based on scientific discovery through an anatomic rationale or on serendipity, the VL of the thalamus replaced the GP as the target of interest [13]. Thus,

14

thalamotomy became the primary surgical procedure for the treatment of PD, starting in the mid-1950s and reaching a peak during the 1960s. Hyperkinetic patients were also operated on in the most anterior part of the VL thalamic nucleus with good results; thus, in practice, pallidotomy was discarded. Ventro lateral-thalamotomy was carried out on patients with PD or other movement disorders throughout the world. However, the accuracy of the surgical procedure at that time fell far short of what is currently being achieved, mainly because imaging analysis was not yet available [14,15]. A common complication arising in surgery was the induction of a movement disorder, hemichorea or hemiballism (Hc/Hb), especially after thalamotomy. Cooper and Bravo analyzed this complication in their patients: 21 patients developed involuntary movements in 850 consecutive BG operations [16]. The patients affected showed a lesion involving the corpus Luysii (subthalamic nucleus STN). After his return to Spain in 1966, Bravo reported that the incidence of Hc/Hb in patients after surgery could be attributed to the placement of the lesion below the intercomissural line. The duration of the disease and the age of patients also became significant factors determining the appearance of complications [17]. He found that no patient over 50 years of age with a disease-duration of less than 10 years developed Hc/Hb. In contrast, patients under 40 years old and with a diseaseduration of more than 10 years developed Hc/Hb after VL thalamotomy, even if the lesion had not reached the subthalamic area [17]. Dr G Dierssen, another Spanish neurosurgeon who trained with Cooper, carried out different studies in the same area, which showed that not all Hc/Hb complications after surgical procedures were due to STN involvement (> Figure 14-1). Dierssen et al first published an account of the case of a 35-year-old parkinsonian patient with severe tremor and rigidity, on whom a right thalamotomy was performed. The patient

181

182

14

History of stereotactic surgery in Spain

. Figure 14-1 Dr Dierssen (front row left in the photograph) with Dr Cooper (second from left) in Brussels in 1958

developed dyskinesia (Hb) hours after surgery, which lasted for days. A second procedure was undertaken to undo the movement induced but the surgical intervention failed and the movement disorder persisted. The patient died of a pulmonary embolism 5 months after the second surgical procedure; an anatomopathological study showed that no lesions were placed in the STN. The first lesion destroyed the VL nucleus, involving the thalamic fasciculus; and the second was placed in the red nucleus and rubro tegmental fibers [18]. This case was also reported by Cooper in his book “The Vital Probe” as case number 1, and by Gioino as case number 6 [19,20].

1960–70 After his return to Spain, Dierssen continued to analyze Hc/Hb in patients with PD who had undergone surgical procedures, developing the diskynesia ipsilateral in thalamotomy [21] and an hemiballism as the primary manifestation of a chiasm-optic nerve glioma in a child [22]. However, the most interesting study, which is not well-known because it was written in Spanish, was the report on 116 Hb with anatomopathological study [23]. In the conclusion, he held that in a high percentage of cases (65%) with Hc/ Hb—not only surgical patients—multiple anatomical structures were affected and the movement

History of stereotactic surgery in Spain

disorder was not always induced by STN involvement; he pointed out that a number of patients with subthalamic lesion showed no clinical sign. A lesion in the striatum or GP may also induce a movement disorder similar to the subthalamic affect [23]. He reported that the percentage of patients developing diskynesia after thalamotomy increased in cases of postencephalitic parkinsonism and after bilateral surgeries [23]. Dierssen returned to the Hospital La Paz with S Obrador and later (1975) moved to Santander, but during that time the number of surgical procedures carried out on patients with PD decreased through the introduction of levodopa as a treatment for the disease. Hundreds of patients with PD were operated on in two different centers in Madrid at that time—the early 1960s—and in Barcelona (Dr Isamat). The procedure was performed with the stereotactic frame (Cooper frame) and ventriculography with lypiodol. The intercommisural line (ICL) was measured and the target was selected in the medial third of the ICL and 11–14 mm from the midline. A leucotome (McKenney) was introduced and opened near the target; patient tremor and rigidity were evaluated intraoperatively. If tremor was arrested, a mixture of lypiodol and hot wax was injected into the target; if tremor persisted, the wire of the leucotome was opened more. Very few papers and reports about Spanish patients operated on during that period of time exist, but a doctoral thesis recorded 200 patients with bilateral thalamotomies (in a group of 1700 patients operated on by Bravo et al) during a 5-year or longer follow-up period in the 1960s and 1970s [24]. The study showed that tremor, rigidity and hypocinesia were stabilized after bilateral surgery, and the benefit persisted for years. Some of the patients presented speech disorders that correlated with the second lesion volume [24]. Stereotactic surgery spread to other Spanish regions when the neurosurgeons returned after their study-periods abroad. In 1969, V Arjona

14

returned from Newcastle (1962–69) (Dr Hankinson) and began to treat parkinsonian patients in Seville with other movement disorders and pain disorders using stereotactic procedures. He had previously spent time with Denise Albe-Fesard and Guiot in Paris, learning about microrecording for target localization. Recording during surgery was a control procedure to place the lesions more accurately and to obtain better results for a long follow-up period. They used a Leksell frame and performed two burr holes: one frontal, for ventriculography and lesioning; the other occipital, for recording. Dr Arjona favored the criogenic lesion because it was reversible, and temperature control was more accurate with this apparatus than in thermolitic procedures. At that time, the target was the ventralis intermedius (Vim) of the thalamus in parkinsonian tremor; the Voa-Vop (Ventralis oralis posterior) was also lesioned in patients with choreo-athetosis or other dyskinesias. Despite the fact that larger lesions were placed, patients with dystonia responded less satisfactorily to thalamic surgery [25]. The surgical target for pain was the Cm-Pf (Centromedianus-Parafascicular) of the thalamus, and the hypothalamus was the target in surgical candidates with aggressivity and oligophrenia erethica [26,27]. Dr JG Martin Rodriguez also performed surgical stereotactic formation with Hankinson in Newcastle (1967–71). He moved to Madrid in 1971, where he developed functional surgery at La Paz Hospital. He acquired extensive experience in thalamic criogenic lesions in patients with PD or other movement disorders. During surgical recording from the occipital cortex, the electrode crossed the internal capsule reaching the GP or VL of the thalamus. Surgical results showed that thalamo-capsular lesions improved tremor, and GP-capsular lesions rigidity [28,29]. During the 1970s, Dr Martin Rodriguez reported on a number of papers about the electrophysiology of the pulvinar nucleus and the role of this anatomical structure in the mechanism of pain

183

184

14

History of stereotactic surgery in Spain

appreciation. He performed pulvinar lesions, combined with other thalamic nuclei (Vop, Vim), in patients with hypertonic-hyperkinetic syndromes; however, the surgical conclusion after patient evolution was not consistent for clinical alleviation [30–32]. In 1972, he and Dr Delgado placed the first electrode with transdermic stimulation in the septal nuclei of the thalamus of a patient with phantom limb pain, by braquial plexus avulsion (see below) [33]. In 1977, Dr Martin Rodriguez moved to the Hospital Santiago Ramo´n y Cajal, but as a result of the positive response to levodopa in patients with PD the number of thalamic surgeries decreased and all stereotactic activity declined. The neurophysiologist, Dr J.M.R. Delgado (et al), developed the technique of implanting multilead electrodes in the brain for several days (> Figure 14-2). The electrodes were made of enameled stainless steel wires or of coated silver wires, which had the advantage of flexibility. Their diameter (0.1–0.2 mm) permitted the insertion of the active portion without isolate for a long period of time [34]. J.M.R. Delgado was . Figure 14-2 Dr Delgado circa 1965

a physiologist who moved to Yale University in 1950; he was to work with Dr J.F. Fulton there for 20 years. After his return to Madrid, he worked with Dr Obrador and Dr J.G. Martin Rodriguez; during the 1960s, they developed a device connected to the electrodes and controlled by radio waves which was able to record neuronal activity and could also enable the stimulation of internal structures. The device was called the “stinoceiver,” and it was tested in different animal species, including a bull. The device was finally implanted in a patient with a phantom limb in 1968 [35]. Electrodes were implanted in the Caudate head and septal nuclei (near accumbens nucleus), bilaterally, through two frontal burr holes. The transdermic stimulation was “on” for a number of hours daily, alleviating patient pain. This may have been the first implantation of a deep brain stimulation device in Europe.

1970s In the early 1970s, Dr G Bravo (> Figure 14-3) and Dr J Miravet, a neurophysiologist in the Clinica Puerta de Hierro in Madrid, designed a operating room (OR) for stereotactic surgery. This OR was built using the Talairach technique for epilepsy study, and their surgical treatment permitted the implantation of multicontact electrodes in stereotactic conditions to record electrical activity during the onset and propagation of seizures (estereoelectroencephalography: SEEG). The operating table could be rotated through 360 to perform ventriculographies with teleradiography, without magnification or distortion in the studies. The Talairach frame permitted their replacement in patients; this approach had the advantage of supplanting different radiological studies, such as angiography and ventriculography. A room with a glass wall next door to the OR was the neurophysiological laboratory, which had 41 electroencephalography

History of stereotactic surgery in Spain

14

. Figure 14-3 Dr Bravo one of the spanish pioneers in the surgical treatment of Parkinson’s disease in his office in Madrid

channels for recording. The room as a whole was electrically insulated. During that period Dr M Manrique spent 2 years in the Delgado lab and later moved to Paris with Dr J Talairach to study electrode placement in patients with epilepsy [36–38]. He and Dr R Garcı´a de Sola went on to develop the surgical treatment of refractory epilepsy in Madrid. These multiple radiological studies enabled the implantation of subdural electrodes, to define the epileptic zone, and their resection with the advantage of superimposed angiography. Later, M Manrique applied stereotactic procedures for epilepsy (stereoelectrocorticography), with reference to subdural electrodes in MRI (magnetic resonance image) in the Talairach gride, and after identification of the anterior and posterior commissures [36,39,40]. The stereotactic study referenced the position of the electrodes and the epileptogenic zone, the different cortical areas and vascular information in the frame space. The information was used during surgery to facilitate accurate resection. In 1977, in the Hospital Santiago Ramo´n y Cajal, a second OR for stereotactic surgery, similar to the one described above, was designed using a Leksell

frame. Dr JG Martin Rodriguez with JC Bustos, F Figueiras in neurosurgery, and E Garcia Austt and W Bun˜o in neurophysiology treated hundreds of patients during that time. Dr Eiras carried out his stereotactic surgical activity in Zaragoza. In 1966, he went to Freiburg in Germany—the Hassler school, with Riechert and Mundinger. These authors described other targets for tremoric parkinsonian patients, such as the zona incerta placed dorsal to the STN, near the fasciculus lenticularis (campotomies). After his return, using the Riechert-Mundinger frame, Dr Eiras performed campotomies in patients with PD, and also targeted the CM-Pf bilateral with asymmetric lesions in patients with pain disorders and Voa-Vop for dystonia. He described a post-traumatic case with action myoclonus that was alleviated through Vop-Vim thalamotomy [41]. Following the introduction of CT (computer tomography), he and his team pioneered the implantation of stereotactic biopsies with frame and the new image tool. They performed tumoral resections with the help of the stereotactic coordinates, using the Robert Wells (Radionics) equipment for these surgical interventions.

185

186

14

History of stereotactic surgery in Spain

The significant clinical impact of the introduction of levodopa therapy for PD during the 1960s brought about a decline in the surgical treatment of movement disorders. In a large number of surgical departments, such surgery practically disappeared. A few neurosurgeons continued to perform the procedure on patients with levodopa intolerance. Sixteen neurosurgeons were questioned by Laitinen in 1985 regarding their preferred target for PD [42]. The responses reveal a variation in the chosen target (VL, zona incerta, Vim, Forel’s field); however, none of the neurosurgeons used GP as the target for PD during the 1980s [42]. During these years in Spain, only one or two teams carried out operations on parkinsonian patients who did not respond to treatment with levodopa. Nowadays, and over the last 15 years, surgery for advanced PD has been revived. The major reasons for this renaissance are the increased understanding of the pathophysiology of the

basal ganglia and the demonstration of surgical alleviation of experimental parkinsonism. In addition, a large proportion of patients suffer severe complications after years of chronic treatment. Moreover, the significant advances in neurosurgery brought about by the introduction of computers and image development, and deep brain stimulation (DBS) that enables low-risk bilateral surgery, are further factors in this regard. However, this new approach in PD surgery centers on a target that had never before been considered: the STN [43].

1970–80 JL Barcia-Salorio, another pioneer in Spanish neurosurgery, worked and carried out stereotaxy in Valencia (> Figure 14-4). He went to Freiburg in 1960, a renowned school at that time, given the participation of Riechert and Toennis;

. Figure 14-4 Dr J L Barcia-Salorio placing the stereotactic frame for a radiosurgical treatment

History of stereotactic surgery in Spain

however, a few months later, he moved to Sweden to work with Prof Leksell in Stockholm and Dr Larsson in Uppsala. His primary intention was to learn about pallidal lesions in patients with movement disorders, but he was very impressed at the Karolinska Institute by the initial steps taken in radiosurgery, using the gamma-knife in different neurosurgical procedures. After Barcia returned to Valencia, he began to carry out stereotactic surgery on parkinsonian patients, above all, pallidotomies; however, he also inaugurated the use of radiosurgical treatment in Spain. Basing his development on the Leksell frame, he designed and built the Barcia frame, capable of supporting the heavy collimators; cobalt was used as the source of radiation in his groundbreaking approach to radiosurgical treatment. He calculated the dose due to a specific target mathematically, and developed a system based on the tomography in AP and lateral to localize a brain lesion using cartesian coordinates, before the technical innovation of CT and MRI. He localized the coordinate position and lesion size through this early procedure, creating a target volume to be treated [44]. In 1975, he performed the first radiosurgical treatment in Spain; this was reported to the ESSFN (European Society of Stereotactic and Functional Neurosurgery) in 1977. In 1979, he described the radiosurgical treatment of large acoustic schwanomas; later (1982), he performed the first treatment of carotid cavernous fistulas (ccf) using radiosurgery [45–48]. He also developed the introduction of low dosages of radiotherapy in patients with resistant epilepsy, who had previously been treated unsuccessfully with a temporal lobectomy [49]. Prof. Barcia’s most significant contribution to neurosurgery was his pioneering study of radiosurgery for ccf with low flow and the treatment of epilepsy. He established the Valencia school that lives on into the present in the work of Dr J Barbera´, Dr J Broseta and Dr P Rolda´n.

14

In 1990, the first LINAC for radiosurgery was installed in the Sanatorio San Francisco de Asis in Madrid, under the direction of Dr Sambla´s and Dr JC Bustos. Today, there are more than 20 LINAC units in Spain; there is also one gamma knife, in the Clinica Ruber in Madrid. As a young Spanish neurosurgeon, J. A. Burzaco (1932–2006) went to Cheshire (England) (1956–57), and later worked in the Walton Hospital in Liverpool as a registrar (1957–58); his contact with L. Leksell in the Serafirmerlassarettat in Stockholm (1961–62) had a decisive impact on his future development in the stereotactic field (> Figure 14-5). He returned to Spain in 1962, practiced surgery in a number of different hospitals in Madrid; he always had a great interest in the neurosurgical treatment of psychiatric diseases. On the basis of Egas Moniz’s description of such surgery in psychiatric patients,

. Figure 14-5 Dr Burzaco, a pioneer figure in psychiatric surgery in Spain also worked with the gamma knife

187

188

14

History of stereotactic surgery in Spain

lobotomies were regularly carried out in Spain at that time. Burzaco combined both approaches: stereotactic surgery and the selection of psychiatric candidates [50]. He reported his experience with thermolesions in the anterior arm of internal capsula (capsulotomies), using the Leksell’s target in patients with obsessive neurosis and severe autoaggressive compulsions, and describing 108 capsulotomies in patients with obsessive compulsive disorders (OCD) [51,52]. Lesions were placed bilaterally and symmetrically, and the follow-up period was either one or 2 years. His results showed a 73% rate of great alleviation (symptom-free or an improvement in normal life); that is, in 62 of the 85 patients on whom he operated. His analysis revealed that improvement was greater among patients who were 30 years old or younger, as compared with patients who were 40 years old or older (83.3% vs. 67%) [51,52]. Dr Burzaco’s most significant contribution to the field of psychiatric surgery was thermolesion in the stria terminalis (fascicle from amygdala to septal nuclei in the hypothalamus) in complex patients experiencing severe character, aggressivity and behavior changes. He first described the technique in a young patient after an encephalitis, but the surgery was later performed on a selection of patients with violent aggressive behavior [53]. The target was placed 3 mm anterior to the anterior commissure, 5–6 mm lateral to the wall of the third ventricle, and at the level of the intercommissural line. However, the complexity of the cases treated led to the formation of combined lesions. The fundus of the stria terminalis lesion was placed in 90% of 116 patients with aggressivity, and a posteromedial hipothalamotomy, a capsulotomy or a cinculotomy was also performed as a complementary target [54]. A second operation was carried out on 27% of the patients, which he himself evaluated as showing a dramatic reduction in aggressive behavior, with no mortality and very few complications. Dr Burzaco was a

pioneer in the field of the surgical treatment of complex cases involving psychiatric disorders, and was renowned for his extensive experience throughout the country. His description of the pathophysiology of aggressivity showed that components of the limbic system (hippocampus and amygdala), as well as cortical areas, such as the orbital and prefrontal cortex, were implicated. His experience led him to conclude that major deafferentization should be carried out to alleviate the clinical condition of chronic psychiatric diseases. A bilateral striae terminalis lesion and—in a high percentage of cases—a bilateral cingulotomy were required to disrupt cortical and deep limbic anatomical pathways in patients with aggressive behavior [54,55].

Final Remarks Stereotactic localization within the brain, using CTor MRI, and the introduction of computers in neurosurgery have marked significant advances in this field. The target may now be visualized in tumors, and may also be recorded in the case of a functional anatomical deep structure. Following target selection, computers automatically introduce the coordinate information of the frame, reducing surgical time with a high degree of accuracy. During the 1970s and 1980s, different neurosurgical departments implemented these techniques for brain biopsies, and later for craneotomies with frame. Tumoral pathology advanced with the help of stereotaxy for years, until the introduction of neuronavigation in neurosurgery in current times. A survey carried out by the Stereotactic and Functional group of the Spanish Society of Neurosurgery (2002) in Spain showed that 50% of departments used stereotaxy and/or neuronavigation for tumoral pathologies; 15 of 34 used stereotaxy alone as a technique; only two groups used neuronavigation without stereotactic frame [56]. At that time, there were 16 Radionics

History of stereotactic surgery in Spain

frames, 14 Leksell, two Barcia, and only one Laitinen and Riecher-Mundinger frame. In 1 year, 656 stereotactic biopsies were performed in thirty-four surgical departments, 125 craneotomies guided by stereotaxy, and 95 cases of cyst or abscess evacuation using frame help. Eleven departments performed functional stereotactic procedures on 115 previously operated PD patients and 10 patients with other movement disorder pathologies. In target planning, nine groups used only TAC, five used MRI, and ten groups fusion image; only one group performed ventriculography for intercommissural reference [56]. Stereotactic and functional neurosurgery is currently one of the major areas in neurosurgery, in Spain, as in other developed countries: its future is wide and open. Current applications and procedures include DBS techniques, ablative procedures, along with drug delivery, gene therapy and cell transplantation in degenerative disorders. The patients involved suffer from PD, essential tremor, dystonia, chorea, multiple sclerosis, pain, epilepsy and psychiatric disorders, such as depression and OCD. Surgical techniques have evolved over the course of many years, but patients continue to suffer the burden of their diseases in ways similar to patients in the past.

Acknowledgments We would like to acknowledge the information provided and opinions shared by M Arra´zola, F Aguilera, V, Arjona, K Buus, M Dierssen, J Eiras, R Figueiras, F Isamat, R Martinez, J Molet, and JG Martı´n Rodriguez.

References 1. Meyers R. Surgical procedure for postencephalitic tremor, with notes on the physiology of the premotor fibers. Arch Neurol Psychiatry 1940;44:455-9.

14

2. Spiegel EA, Wycis HT, Marks M, Lee AJ. Stereotaxic apparatus on the human brain. Science 1947;106:349-50. 3. Obrador S. Personal recollections of the development of human stereotactic neurosurgery. Confinia Neurol 1975;37:378-83. 4. Obrador S, Dierssen G. Cirugı´a de la regio´n palidal en el sı´ndrome de Parkinson. Te´cnica personal y resultados inmediatos en los seis primeros casos operados. Revista Clı´nica Espan˜ola 1956;61:229-37. 5. Obrador S. A simplified neurosurgical technique for approaching and damaging the region of the globus pallidus in Parkinson’s disease. J Neurol Neurosurg Psychiatr 1957;20:47-9. 6. Obrador S, Dierssen G. Results and complications following one hundred subcortical lesions performed in Parkinson’s disease and other hyperkinesias. Acta Neurochi 1959;7:206-13. 7. Cooper IS. Surgical treatment of parkinsonism. Ann Rev Med 1965;16:309-30. 8. Cooper IS, Bravo G. Chemopallidectomy and chemothalamectomy. J Neurosurg 1958;15:244-56. 9. Bravo GJ, Cooper IS. Chemopallidectomy: two recent technical additions. J Am Geriatr Soc 1957;5:651-5. 10. Bravo GJ, Cooper IS. A clinical and radiological correlation of the lesions produced by chemopallidectomy and chemothalamectomy. J Neurol Neurosurg Psychiatr 1959;22:1-10. 11. Hassler R. The pathological and pathophysiological basis of tremor and parkinsonism. Second International Congress of Neuropathology, Excerpta Medical Foundation 1955;1:29-40. 12. Hassler R, Riechert T. Indikationen und Lokalisationsmethode der gezielten Hirnoperationen. Nervenarzt 1954;25:441-7. 13. Guridi J, Lozano AM. A brief history of Pallidotomy. Neurosurgery 1997;41:1169-83. 14. Smith MC. Location of stereotactic lesions confirmed at necropsy. Br Med J 1962;1:900-6. 15. Cooper IS, Bergmann LL, Caracalos A. Anatomic verification of the lesion which abolishes parkinsonian tremor and rigidity. Neurology 1963;13:293-315. 16. Schachter JM, Bravo G, Cooper IS. Involuntary movement disorders following basal ganglia surgery in man. J Neuropathol Exp Neurol 1960;19:228-37. 17. Bravo G, Parera C, Seiquer G. Neurological side-effects in a series of operations of the basal ganglia. J Neurosurg 1966;24:640-7. 18. Dierssen G, Bergmann L, Gioino L, Cooper IS. Hemiballism following surgery for Parkinson’s disease. Arch Neurol 1961;5:627-37. 19. Cooper IS. The vital probe: my life as a brain surgeon. New York: Norton; 1981. p. 293-315. 20. Gioino GG, Dierssen G, Cooper IS. The effect of subcortical lesions on production and alleviation of hemiballic and hemichoreic movements. J Neurol Sci 1966;3:10-36.

189

190

14

History of stereotactic surgery in Spain

21. Dierssen G, Gioino G, Cooper IS. Participation of ipsilateral hemisphere lesions in the pathology of hemichorea and hemiballismus. Neurology 1961;11:894-8. 22. Dierssen G. Sobre un caso de hemibalismo producido por un glioma de ta´lamo o´ptico. Rev Clinica Espan˜ola 1962;84:339-42. 23. Dierssen G, Gioino G. Correlacio´n anatomica del hemibalismo. Rev Clin Esp 1961;82:283-305. 24. Herrero J. Resultados tardı´os de la cirugı´a en la enfermedad de Parkinson. Situacio´n clı´nica de 200 enfermos despue´s de cinco o ma´s an˜os de haber sido operados bilateralmente. Doctoral Thesis, Universidad Autonoma de Madrid; 1980. 25. Burzaco J. Stereotactic pallidotomy in extrapyramidal disorders. Appl Neurophysiol 1985;48:283-7. 26. Arjona V, Hankinson J. Cirugı´a tala´mica del dolor. Rev Clin Espa 1969;113:313-22. 27. Arjona VE, Martin-Rodriguez JG. Cryohypothalamotomy for the treatment of aggressive behavior in oligophrenia erethica. Neurological surgery. Amsterdam: Excerpta Medica; 1978. p. 320-4. 28. Gillingham FJ, Watson WS, Donaldson AA. The surgical treatment of parkinsonism. Brit Med J 1960;12 Nov:1395-402. 29. Gillingham FJ, Kalyanaraman S, Donaldson AA. Bilateral stereotaxic lesions in the management of parkinsonism and the dyskinesias. Brit Med J 1964;2:656-9. 30. McComas AJ, Wilson P, Martin-Rodriguez JG, Wallace AC, Hankinson J. Properties of somatosensory neurons in the human thalamus. J Neurol Neurosurg Psychiatr 1970;33:716-7. 31. Martin-Rodriguez JG, Bun˜o W, Jr, Garcia-Austt E. Human pulvinar units, spontaneous activity and sensorymotor influences. Electroenceph Clin Neuropath 1982;54:388-98. 32. Martin-Rodriguez JG, Obrador S. Evaluations of stereotaxic pulvinar lesions. Conf Neurol 1975;37:56-62. 33. Obrador S, Delgado JMR, Martin-Rodriguez JG, SantoDomingo, Alonso A. Estimulacio´n cerebral transdermica en miembro fantasma doloroso. Revista espan˜ola de OtoNeuro-Oftalmologı´a y Neurocirugı´a 1972;30:269-72. 34. Delgado JMR. Permanent implantation of multilead electrodes in the brain. Yale J Biol Med 1952;24:351-8. 35. Delgado JMR, Mark V, Sweet W, Erwin F, Weiss G, et al. Intracerebral radio stimulation and recording in completely free patients. J Nerv Ment Dis 1968;147:329-40. 36. Talairach J, Peragut JC, Farnarier P, Manrique M. The role of the stereotactic radiographic exploration in neurosurgical interventions. In: Salomon GG, editor. Advances in cerebral angiography. Berlin: Springer; 1976. p. 272-3. 37. Manrique M, Alborch E and Delgado JMR. Cerebral blood flow and behavior during brain stimulation in the goat. Am J Physiol 1977;232:495-9.

38. Bancaud J, Talairach J, Geier S, Bonis A, Trorrier S, Manrique M. Manifestations comportamentales induites par la stimulation electrique du gyrus cingulaire anterior chez l’homme. Rev Neurol (Paris) 1976;10:705-24. 39. Manrique M, Rodriguez Albarin˜o M, De la Torre M, Blazquez MG. Stereocorticography in the surgical treatment of epilepsy. Stereot and Funct Neurosurg 1994;63 (1–4):101. 40. Manrique M, Parera C, Nombela L, Miravet J, Bravo G. Stereotaxic radiographic and computerized axial tomographic explorations in the surgical treatment of epilepsy. Presented at the third meeting of European Society for Stereotactic and Functional Neurosurgery (ESSFN). Freiburg 1977. 41. Eiras J. Sı´ndrome mioclo´nico postrauma´tico. Efectividad de las lesiones tala´micas sobre las mioclonı´as de accio´n. Arch Neurobiol 1980;43:17-28. 42. Laitinen LV. Brain targets in surgery for Parkinson’s disease. Results of a survey of neurosurgeons. J Neurosurg 1985;62:349-51. 43. Guridi J, Luquin MR, Herrero MT, Obeso JA. The subthalamic nucleus: a possible target for stereotaxic surgery in Parkinson’s disease. Mov Disord 1993;8:421-9. 44. Barcia-Salorio JL, Barbera´ J, Broseta S, Soler F. Tomography in stereotaxis. A new stereoencephalotome designed for this propose. Acta Neurochir 1977;Suppl 24:77-83. 45. Barcia Salorio JL. Radiosurgical treatment of huge acoustic neurinomas. In: Szikla, editor. Proceedings of the inserm symposium No. 12, 1979. Oxford, UK: Elsevier; p. 245-9. 46. Barcia-Salorio JL, Hernandez G. Stereotactic radiosurgery in acoustic neuninomas. Acta Neurochir 1984;Suppl 33:373-6. 47. Barcia Salorio JL, Hernandez G, Broseta J. Radiosurgical treatment of carotid-cavernous fistula. Appl Neurophysiol 1982;45:520-2. 48. Barcia-Salorio JL, Roldan P, Hernandez G. Radiosurgical treatment of epilepsy. Appl Neurophysiol 1985;48:400-3. 49. Barcia Salorio JL, Soler F, Hernandez G. Radiosurgical treatment of low flow carotid-cavernous fistulae. Acta Neurochir 1991;Suppl 52:93-5. 50. Burzaco JA, Gutierrez Gomez D. Trastorno de conducta postencefalitico (su tratamiento por cirugia estereotaxica). Archivos de Neurobiologia 1968;31:69-77. 51. Lopez-Ibor JJ, Burzaco J. Stereotaxic anterior limb capsulotomy in selected psychiatric patients. In proceedings of the second international conference in psychosurgery, Copenhagen, Denmark, Springfield, IL: Charles Thomas Publishers; 1970. p. 391-9. 52. Lopez-Ibor JJ, Lopez-Ibor JA, Burzaco JJ, Duque del Rio M. Capsulotomia esterotaxica. Indicaciones y Resultados. Actas Luso Espan˜olas de Neurologı´a Psiquiatrica y Ciencias Afines 1974;3:219-24. 53. Burzaco JA. Fundus Striae terminalis, an optional target in sedative stereotactic surgery. Surgical Approaches in Psychiatry. In: Laitinen L, editor. Third international

History of stereotactic surgery in Spain

congress of psychosurgery. Chapter 20, Lancaster: MTP; 1973. p. 135-7. 54. Burzaco J. The role of some limbic structures in aggressive behavior. In: Gris P, Struwe G, Jansson B, editors. Elsevier. North-Holland. Biomedical Press. Biological psychiatry; 1981. p. 1223–1126.

14

55. Burzaco JA. Stereotactic surgery in severe unresponsive aggressive syndromes. Biological Psychiatry Vol. 2 Ed Racagni. Elsevier Science Publishers BV; 1991. p. 241–244. 56. Guridi J. Stereotactic neurosurgery in Spain. Neurocirugı´a 2002;13:406.

191

3 History of Stereotactic Surgery in US P. L. Gildenberg

The early use of functional neurosurgery was begun by Horsley [1] in England at the end of the nineteenth century, and the invention of stereotactic surgery in animals was begun by Horsley and Clarke [2] at the beginning of the twentieth century. Human stereotactic surgery began almost at mid-century, i.e., 1947, in the United States by Ernest A. Spiegel and Henry T. Wycis [3] at Temple Medical School in Philadelphia. Stereotactic surgery was accepted at so many institutions so quickly that it is difficult to identify individual ‘‘schools’’ of stereotactic surgery, as it is in other countries. Indeed, in the early 1960s many neurosurgeons, who did not publish, were practicing functional neurosurgery, but most quickly left the field when L-dopa was introduced near the end of that decade [4] and have not returned to the field [5]. In the first half of the twentieth century, prior to the introduction of human stereotaxis, several American functional neurosurgeons were dominant in the use of non-stereotactic techniques for movement disorders. Paul Bucy, in Chicago, recommended motor cortex extirpation or corticospinal tractotomy for the treatment of athetosis [6] and Parkinson’s disease [7]. Bucy [7,8] had declared well into the 1950s that it was necessary to damage the corticospinal system in order to achieve relief from involuntary movements. Dandy [9], based on observation of several patients with intracerebral hemorrhage, had averred that damaging the extrapyramidal system would result in permanent intractable coma. Earl Walker, of Johns Hopkins, reported a pedunculotomy wherein he sectioned the lateral #

Springer-Verlag Berlin/Heidelberg 2009

two-thirds of the peduncle for relief of hemiballismus [10] or parkinsonian tremor [11]. It was in attempting the Walker procedure that Irving Cooper had his famous ‘‘surgical accident,’’ where he accidentally cut the anterior choroidal artery and found the patient much improved, which led him to advocate ligation of that vessel for treatment of movement disorders [12], as discussed below. The most important but often overlooked American functional neurosurgeon of the prestereotactic era is Russell Meyers of the University of Iowa. It was his pioneering work that proved both Paul Bucy and Walter Dandy wrong. In 1939, Meyers [13,14] performed a craniotomy and transventricular approach to resect the head of the caudate nucleus for successful treatment of Parkinsonian tremor. His observations were presented at a meeting of the Research Association for Nervous and Mental Disease the following year [14], where a number of senior members encouraged him to pursue these observations, which led to the publication of results in 39 patients operated with various open surgical procedures of the basal ganglia [15]. The results were good, but the mortality rate was so high that even Meyers recommended against such surgery. His observations, however, were critical to defining the first extrapyramidal targets, significant information that led directly to the first stereotactic surgery for a movement disorder, Huntington’s chorea, with the pallidum as the target [3]. Stereotactic surgery produced even better results and brought the mortality rate down to 1% within 3 years of its introduction [16]. In 1963, Meyers resigned his appointment

46

3

History of stereotactic surgery in US

at the University of Iowa, reportedly for personal reasons, and became Chief of Neurosurgery of the Appalachian Regional Hospital at Williamson, West Virginia. It was not uncommon thereafter for the question to be raised at each Stereotactic Society Meeting, ‘‘Whatever happened to Russell Meyers?’’ Ernest A. Spiegel (> Figure 3-1) graduated from the University of Vienna, where he remained on the faculty both as a neurologist and laboratory scientist. As anti-Semitism advanced in Austria during the 1930s, he found himself with fewer students and restricted access to his laboratory. A businessman who observed this on a trip to Vienna related Spiegel’s plight to Dr. William Parkinson, the Dean of Temple Medical School, who invited not only Ernest Spiegel but also his wife, Mona Spiegel-Adolph, PhD, Professor of Colloid Chemistry, to join the faculty in Temple, where they both worked until retirement. Spiegel was small in stature, with wirerimmed glasses, a somewhat unkempt look, and a thick accent which identified him as a professor

steeped in the European academic philosophy. He remembered everything, and as he wrote his manuscripts (usually with a pencil stub on the back of used EEG paper), he inserted the citations without the need to consult his library. His laboratory consisted of two small and cramped rooms – one lined with shelves that contained an uncounted number of cat brains in baby food jars and the other containing a Faraday cage for recording. Inside the cage was an animal stereotaxic apparatus on a small table. Although many considered Spiegel severe because of his professorial look, he had a wry sense of humor, which was a necessary trait to work with Henry T. Wycis, who was a practical joker. Henry Wycis (> Figure 3-2) was incorrigible. He came from a middle class family, and helped supplement his living expenses by playing semiprofessional baseball during college, which seemed remarkable, because he weighed over 300 pounds by the time I met him. He began to work with Spiegel when he was a medical student – although his academic record was unsurpassed for many years, he also held the record

. Figure 3-1 Ernest A. Spiegel

. Figure 3-2 Henry T. Wycis

History of stereotactic surgery in US

for having missed the most classes, which may have accounted for his time in Spiegel’s laboratory. They continued to work together while Wycis was a neurosurgical resident at Temple and after he had joined the faculty. Just the opposite of Spiegel, Henry Wycis loved to be with a diverse group of people. He enjoyed doing card tricks for his friends. It was rumored that he had earned his way through Medical School by successfully playing poker, which may be because of his photographic memory or may explain his love of card tricks. After stereotactic techniques were introduced in 1947 [3], many neurosurgeons visited Spiegel and Wycis at Temple Medical School in Philadelphia to learn of this new field and return home to make their own apparatus, (since none were commercially available for approximately the next decade,) and become practitioners of this new discipline. Although many of the visitors were from Europe, many were also US neurosurgeons. Even though the field was born in the US, the stereotactic community was and remains truly an international community. Those most active in the field during the 1950s, probably fewer than 30 surgeons, met irregularly at various institutions. The information exchange was informal, open, and enthusiastic, since those scientists shared the excitement of participating in a new science. The first patient reported by Spiegel and Wycis in 1947 [3] had Huntington’s chorea. His involuntary movements became more severe when he was stressed. Consequently, two lesions were made, one in the globus pallidus for the involuntary movement and one in the dorsomedial nucleus of the thalamus to lessen the stress reaction. Lesions were made with alcohol injection, in hopes of sparing the fibers en passage. The next patients had lesions made with a direct current, which had been described in detail in Horsley and Clarke’s original animal stereotaxis paper [2]. Spiegel and Wycis concluded their paper by commenting, ‘‘the apparatus is being

3

used for psychosurgery. . . Lesions have been placed in the region of the medial thalamus. . .Further applications of the stereotaxic technique are under study, e.g., interruption of the spinothalamic tract in certain types of pain or phantom limb; production of pallidal lesions in involuntary movements; electrocoagulation of the Gasserian ganglion in trigeminal neuralgia; and withdrawal of fluids from pathological cavities, cystic tumors.’’ Spiegel was somewhat secretive about future plans, and I am certain that they had already done those procedures prior to the first publication. I first met Spiegel and Wycis during my freshman year at Temple Medical School. A new summer research program had been announced, and I was looking for someone in the neurological sciences to be my sponsor and guide my research. I was referred by the head of physiology, since there was no neurophysiologist in that department I walked into Spiegel’s laboratory to find him and Wycis reviewing pre- and postoperative 8-mm motion picture films of patients. They invited me to sit and watch, and 2 hours later I was accepted as Spiegel’s graduate student. This was in the spring of 1956, just 9 years since the field of stereotactic surgery had begun, when it was still in its infancy. Spiegel and Wycis then performed surgery on only one patient per week. Targeting required a pneumoencephalogram, which was performed with the apparatus in place on Tuesday. The patient was so sick from the study that the surgical part was delayed until Thursday, when the apparatus was re-applied and the procedure done. Every time an electrode was inserted into the brain of an awake patient was an opportunity to study human neurophysiology, which both helped our understanding of the human extrapyramidal nervous system and provided physiologic confirmation that the electrode was at the intended target. In 1968, the International Society for Research in Stereoencephalotomy was formed, along with the American and European

47

48

3

History of stereotactic surgery in US

Branches. The officers of the American Branch, which included both Canada and the United States, included Ernest Spiegel as President, Lyle French as Vice President, and Henry Wycis as Secretary-Treasurer. Claude Bertrand of Montreal was the sole Canadian member of the Board, and served along with Blaine S. Nashold, Jr., Vernon Mark, Robert W. Rand, and Orlando Andy. At the next official meeting in 1970, those same neurosurgeons remained officers, an indication of how small the membership was, with French as the President, and the non-neurosurgeon Spiegel resigned from his office. At the next meeting in 1972, John Alksne was a new member of the Board, in place of Lyle French. The organization was revamped in 1973 as the World Society for Stereotactic and Functional Neurosurgery, and the American Society for Stereotactic and Functional Neurosurgery (as well as the European Society) were formed. It was by that time 25 years since the introduction of stereotactic surgery, and each of the founders had taught a number of trainees, so the field had been expanding rapidly. The officers of the American Society retained Blaine Nashold as President and Claude Bertrand as Vice-President. I took over as Secretary shortly after Henry Wycis’ death in 1972, and held that position in both the American Society and the World Society for the next 28 years, except for the years I was President of the American Society from 1977 to 1980 and President of the World Society for Stereotactic and Functional Neurosurgery from 1993 to 1997. The evolution of stereotactic and functional neurosurgery in the United States took a somewhat different course than in most of the rest of the world. Up until the last decade, most stereotactic surgeons performed such surgery as part of a general neurosurgical practice, or one which also featured other subspecialties. There were few ‘‘stereotactic centers,’’ even in universities, as was the norm in other countries where medicine

was directed by government or academic agencies. Both medical school and private neurosurgical practitioners devoted part of their practice to stereotaxis, but also performed other neurosurgery, as well. This is in contrast to the last decade, where more sophisticated technology requires a team, so that multispecialty stereotactic services are more common, usually centered around teaching programs, such as Pat Kelly at NYU, Ali Rezai at the Cleveland Clinic, and others. In the pre-dopa days, the largest functional neurosurgical practice in the US was that of Irving Cooper, who devoted his practice to functional neurosurgery after the mid-1950s [17]. He embarked on functional neurosurgery because of a ‘‘surgical accident’’ [12]. He was performing a Walker [11] pedunculotomy for Parkinson’s disease, when he accidentally cut the anterior choroidal artery. He aborted the procedure, but the patient awoke with marked improvement. That led Cooper to advocate ligation of that vessel for the treatment of Parkinson’s disease [12]. The distribution of that artery, however, is very variable, and so were the results of its ligation. By that time, the pallidum had become a common target for stereotactic treatment of parkinsonism [18], so Cooper advocated injecting alcohol into that structure in so-called chemopallidectomy [19]. Again the results were variable, since the insertion of the needle was free-hand and the alcohol spread in an uncontrolled fashion along the adjacent tracts. He tried using a thicker solution, Etopalin, and a cannula with a balloon at the end in hopes of making a cavity that would contain the injected solution [20]. Neither of these maneuvers produced a more predictable lesion [21,22]. Finally, he recruited a freelance engineer, Arnold StJ. Lee, who designed the cryoprobe, which used a controlled release of liquid nitrogen through a probe to freeze the tissue at the tip [23]. Although it had a large blunt tip that injured tissue on insertion, it produced a predictable lesion at the tip. It was purely coincidence

History of stereotactic surgery in US

that the engineer who built the Cryoprobe was the same Lee who is the fourth author on the first stereotactic paper by Spiegel and Wycis [3] in 1947. Cooper used an aiming device that was not truly stereotactic, in that it was not based on a Cartesian system. He approached the pallidum by inserting a cannula ventral and medial through the temporal lobe. One of his patients, who had an excellent result, was killed in an accident. An autopsy involving the brain showed that the lesion was in the ventrolateral thalamus, a target that had already been described as preferable for tremor. Cooper changed his target to that structure and reported another large series of chemopallidectomy. Cooper brought functional neurosurgery, including stereotactic surgery, to the public through the mass media. One of his patients was Margaret Bourke-White, the famous Life magazine photographer who suffered from Parkinson’s disease. She insisted that her surgery be photographed by one of her colleagues, Alfred Eisenstadt, who was equally famous. Her procedure and result were excellent, and the pictures and article in a mass circulation magazine brought considerable attention to Dr. Cooper and to stereotactic and functional neurosurgery. There have been persistent stories about clashes between Cooper and Wycis at stereotactic meetings. Some of the more colorful stories had them coming to physical blows. Not only is that not true, as far as I can document, but that competition would have gone to Wycis. He was a bear of a man, who weighed more than 300 pounds, and was a semi-professional athlete in his college years. There certainly were verbal assaults, however, and a sense of one-upmanship when they disagreed. I was present at a stereotactic meeting at Temple Medical School in 1958, when such a competition occurred. Cooper brought one his successful patients to the meeting to show how well he could write on a blackboard after surgery. Not to be outdone,

3

Henry Wycis brought a patient to the meeting the following day to demonstrate how well he played the piano after a pallidotomy. We have lost much of the color of those early meetings. There has been a recent shift toward implanting deep brain stimulators, but story actually began in the late 1960s. The development of the majority of neuromodulation devices presently used occurred in the United States, mainly through Medtronic1, that remains the dominant supplier of implantable stimulators [24]. The introduction of the gate theory by Melzack and Wall [25] in 1965 led Norm Shealy, a neurosurgeon at Western Reserve Medical School (now Case Western Reserve) in Cleveland, to consider stimulating the dorsal columns of the spinal cord to ‘‘close the gate’’ for relief of chronic pain [26]. He worked with Tom Mortimer, who previously had spent time working at an American company, Medtronic1, that at time had several implantable stimulators on the market. Their Barostat stimulator that was used for stimulation of the carotid nerve for management of hypertension in 1963 and their Angiostat in 1965 to treat angina, were adapted to electrodes designed by Mortimer to stimulate the spinal cord, and the field of neuromodulation using commercially available implantable stimulators was born [24]. Shealy left neurosurgery soon thereafter to become a horse rancher in Wisconsin and write mystery books. It was in 1973 that Hosobuchi [27], then at the University of California at San Francisco, inserted an electrode into the somatosensory thalamus to treat denervation pain, and deep brain stimulation became a reality. Shortly after that, Don Richardson [28,29], of Tulane in New Orleans, stimulated the periaqueductal area for management of somatic pain. At around the end of the 1970s, the use of deep brain stimulation required approval by the FDA, but only one of the three companies manufacturing implantable stimulators performed the necessary studies to document its benefit in pain; the third company

49

50

3

History of stereotactic surgery in US

was Avery, who obtained approval, but their founder, Roger Avery, retired just at that time, so the use of deep brain stimulators was deapproved. The use of deep brain stimulation ceased in the US. It was not until the use of implantable deep brain stimulators for motor control was documented by Alim Benabid [30] and later by Jean Siegfried [31], colleagues in Europe, that there has been a re-ignition of DBS activity in US centers. This led to the reapproval of DBS for movement disorders by the FDA in early 2002. Lars Leksell [32,33] introduced the Gamma Knife for stereotactic radiosurgery in Stockholm. The first unit installed in the United Staates was guided through the vast regulatory bureaucracy by Dade Lunsford [34] at the University of Pittsburgh, which became one of the most active Gamma Knife centers anywhere. Once the regulatory problems had been addressed by Lunsford, many Gamma Knives were imported into the US, sometimes directed by neurosurgeons who had previously worked in Sweden, such as Ladislau Steiner at the University of Virginia and Georg Noren at Rhode Island Hospital. Although linear accelerator stereotactic radiosurgery was invented by Leksell [32] in Europe, he used primarily his Gamma Knife. Later Betti [35] and Colombo [36] reintroduced the linac for radiosurgery. Several US neurosurgeons also became active in that time when the benefits of radiosurgery were becoming apparent, but there were few Gamma Knives in this country. Linac systems were developed at the University of Florida at Gainesville by William Friedman and Frank Bova [37]. Several neurosurgeons including Peter Heilbrun were involved in development of the Radionics XKnife, which was first used at the Joint Center in Boston by Jay Loeffler [38]. The use of proton beam therapy was reported by Ray Kjellberg [39] as early as 1962. During the past few years, a Proton Beam Center was opened at Loma Linda and more recently at the MD Anderson Cancer Center in Houston.

Pain management has always been a major interest of US neurosurgeons. An appreciation for the evolving philosophy of neurosurgical management of pain can be obtained by perusing the three volumes co-authored by William Sweet, who was the epitome of professorship. The first was by James White and Sweet [40] in 1955, which emphasized the interruption of the primary pain pathways. The second by those same authors appeared in 1969 [41], and provided a somewhat more conservative approach that included the extralemniscal pathways, as well. The third by Jan Gybles of Belgium and Sweet [42] in 1989 emphasized the complexities of pain perception as a guide to management. Anterolateral cordotomy was simplified by Sean Mullan [43], who in 1963 reported a technique of lesioning that part of the spinal cord by percutaneous insertion of a strontium needle at the C1–2 level for a measured duration. The technique was further modified in 1965 by Hu Rosomoff [44], who used a radiofrequency lesion to interrupt the lateral spinothalamic tract, making it accessible to most neurosurgeons. Paul Lin and I [45,46] introduced a technique that introduce the needle through a lower cervical disk, thus avoiding fibers concerned with respiration. It is more than coincidence that the two neurosurgeons with the largest series of percutaneous cervical cordotomies, Rosomoff and I, came to recommend a very conservative approach to surgery and favored comprehensive multidisciplinary management of chronic pain [47,48]. Both of our programs resembled the comprehensive pain management program pioneered at the University of Washington in Seattle, which was led by the anesthesiologist John Bonica [49], and the neurosurgeon John Loeser [50,51]. Interest in stereotactic and functional neurosurgery has been increasing in the United States, especially since the use of deep brain stimulation for motor disorders became available in 2002. The field is of interest to neurologists

History of stereotactic surgery in US

and neurophysiologists, as well as neurosurgeons, which fostered a team approach to management of Parkinson’s disease and other movement disorders. This has developed to the point where the use of intraoperative microelectrode recording has become the norm. Not only has the field become more active, but the scientific basis of the diseases and techniques are being studied with increased intensity in order to assure further progress. Because of the increased complexity and sophistication of electrode implantation, many multidisciplinary centers have developed in the US, such as David Roberts at the DartmouthHitchcosk Medical Center, Michael Kaplitt at Weill Cornell Medical College in New York, Pat Kelly at New York University, Ali Rezai at the Cleveland Clinic, Ray Bakay in Atlanta and then Chicago, then Robert Gross in Atlanta, Michael Schulder in Manhasset, NY, Philip Starr and Nicholas Barbaro at the University of California in San Francisco, Jamie Henderson at Stanford, Tony DeSalles and Mike Apuzzo in Los Angeles, and Kim Burchiel in Portland Oregon, to name but a few. In 1987 I asked, ‘‘Whatever happened to stereotactic surgery?’’ [5] The answer is, ‘‘It is doing well and advancing at an unprecedented rate.’’

References 1. Horsley V, Taylor J, Colman WS. Remarks on the various surgical procedures devised for the relief or cure of trigeminal neuralgia (tic douloureaux). BMJ 1891;2:1139-43. 2. Horsley V, Clarke RH. The structure and functions of the cerebellum examined by a new method. Brain 1908;31:45-124. 3. Spiegel EA, Wycis HT, Marks M, Lee AS. Stereotaxic apparatus for operations on the human brain. Science 1947;106:349-50. 4. Cotzias GC, VanWoert MH, Schiffer LM. Aromatic amino acids and modification of parkinsonism. N Eng J Med 1967;276:374-9. 5. Gildenberg PL. Whatever happened to stereotactic surgery? Neurosurgery 1987;20:983-7.

3

6. Bucy PC, Buchanan DN. Athetosis. Brain 1932;55:479-92. 7. Bucy PC, Case TJ. Tremor. Physiologic mechanism and abolition by surgical means. Arch Neurol Psychiat 1939;41:721-46. 8. Bucy PC. Cortical extirpation in the treatment of involuntary movements. In: Putnam TJ, editor. The Diseases of the Basal Ganglia. New York: Hafner Publishing Co.; 1966. p. 551-95. 9. Meyers R. Dandy’s striatal theory of the ‘‘center of consciousness’’; Surgical evidence and logical analysis indicating its improbability. Arch Neurol Psychiat 1951;65:659-71. 10. Walker AE. Cerebral pedunculotomy for the relief of involuntary movements. I. Hemiballismus. Acta Psychiatr Neurol Scand 1949;24:712-29. 11. Walker AE. Cerebral pedunculotomy for the relief of involuntary movements. Parkinsonian tremor. J Nerv Ment Dis 1952;116:766-75. 12. Cooper IS. Ligation of the anterior choroidal artery for involuntary movements of parkinsonism. Psychiat Quart 1953;27:317-9. 13. Meyers R. Surgical procedure for postencephalitic tremor, with notes on the physiology of premotor fibers. Arch Neurol Psychiat 1940;44:455-9. 14. Meyers R. The modification of alternating tremors, rigidity and festination by surgery of the basal ganglia. Res Publ Ass Res Nerv Ment Dis 1942;21:602-65. 15. Meyers R. Historical background and personal experiences in the surgical relief of hyperkinesia and hypertonus. In: Fields W, editor. Pathogenesis and treatment of parkinsonism. Springfield, IL: Charles C Thomas; 1958. p. 229-70. 16. Gildenberg PL. Neurosurgical treatment of movement disorders: history and update. In: Germano I, editor. Neurosurgical treatment of movement disorders. New York: Thieme; 2002. p. 139-47. 17. Cooper IS. Results of 1000 consecutive basal ganglia operations for parkinsonism. Ann Intern Med 1960;52:483-99. 18. Hassler R, Riechert T. Indikationen und Lokalisationsmethode der gezielten Hirnoperationen. Nervenarzt 1954;25:441-7. 19. Cooper IS. Chemopallidectomy. Science 1955;121:217. 20. Cooper IS, Bravo G, Riklan M, Davidson N, Gorek E. Chemopallidectomy and chemothalamectomy for parkinsonism. Geriatrics 1958;13:127-47. 21. Gildenberg PL. Studies in stereoencephalotomy. VIII. Comparison of the variability of subcortical lesions produced by various procedures (radio-frequency coagulation, electrolysis, alcohol injection). Confin Neurol 1957;17:299-309. 22. Gildenberg PL. Study of methods of producing subcortical lesions and of evaluating their effect upon the tremor of parkinsonism. MS Thesis (Experimental Neurology), Temple University, Philadelphia, PA; 1959. 23. Cooper IS, Lee A St.J. Cryostatic congelation. J Nerv Ment Dis 1961;133:259-63.

51

52

3

History of stereotactic surgery in US

24. Gildenberg PL. Evolution of neuromodulation. Stereotact Funct Neurosurg 2005;83:71-9. 25. Melzack R, Wall PD. Pain mechanisms: a new theory. Science 1965;150:971-9. 26. Shealy CN, Mortimer JT, Reswick JB. Electrical inhibition of pain by stimulation of the dorsal columns. Preliminary clinical report. Anesth Analg (Cleve) 1967;46:489-91. 27. Hosobuchi Y, Adams JE, Rutkins B. Chronic thalamic stimulation for the control of facial anesthesia dolorosas. Arch Neurol 1973;29:158-61. 28. Richardson DE, Akil H. Pain reduction by electrical brain stimulation in man. Part 1: acute administration in periaqueductal and periventricular sites. J Neurosurg 1977;47:178-83. 29. Richardson DE, Akil H. Pain reduction by electrical brain stimulation in man. Part 2: chronic self-administration in the periventricular gray matter. J Neurosurg 1977;47:184-94. 30. Benabid AL, Pollak P, Hommel M, Gaio JM, de Rougemont J, Perret J. Treatment of Parkinson tremor by chronic stimulation of the ventral intermediate nucleus of the thalamus. Rev Neurol (Paris) 1989;145:320-3. 31. Siegfried J. Effect of stimulation of the sensory nucleus of the thalamus on dyskinesia and spasticity. Rev Neurol (Paris) 1986;142:380-3. 32. Leksell L. The stereotaxic method and radiosurgery of the brain. Acta chir scand 1951;102:316-9. 33. Leksell L. Stereotaxis and radiosurgery: an operative system. Springfield, IL: Charles C Thomas; 1971. 34. Lunsford LD, Maitz A, Lindner G. First United States 201 source cobalt-60 gamma unit for radiosurgery. Appl Neurophysiol 1987;50:253-6. 35. Betti O, Derechinsky V. Hyperselective encephalic irradiation with a linear accelerator. Acta Neurochir Suppl 1984;33:385-90. 36. Avanzo RC, Chierego G, Marchetti C, Pozza F, Colombo F, Benedetti A, Zanardo A. Stereotaxic irradiation with a linear accelerator. Radiol Med (Torino) 1984; 70:124-9. 37. Friedman WA, Bova F. The University of Florida radiosurgery system. Surg Neurol 1989;32:334-42.

38. Loeffler JS, Alexander E, III, Siddon RL, Saunders WM, Coleman CN, Winston KR. Stereotactic radiosurgery for intracranial arteriovenous malformations using a standard linear accelerator. Int J Radiat Oncol Biol Phys 1989;17:673-7. 39. Kjellberg RN, Koehler AM, Preston WM, Sweet WH. Stereotaxic instrument for use with the Bragg peak of a proton beam. Conf Neurol 1962;22:183-9. 40. White JC, Sweet WH. Pain, its mechanism and neurosurgical control. Springfield, IL: Charles C Thomas; 1955. 41. White JC, Sweet WH. Pain and the neurosurgeon. A forty year experience. Springfield, IL: Charles C Thomas; 1969. 42. Gybels JM, Sweet WH. Neurosurgical treatment of persistent pain. Physiological and pathological mechanisms of human pain. Pain Headache 1989;11:1-402. 43. Mullan S, Harper PV, Hekmatpanah J, Torres H, and Dobben G. Percutaneous interruption of spinal pain tracts by means of a strontium-90 needle. J Neurosurg 1963;20:931-9. 44. Rosomoff HL, Carrol F, Brown J, Sheptak P. Percutaneous radiofrequency cervical cordotomy: technique. J Neurosurg 1965;23:639-44. 45. Gildenberg PL, Lin PM, Polakoff PP II, Flitter MA. Treating intractable pain with percutaneous cervical cordotomy. GP 1968;37:96-7. 46. Lin PM, Gildenberg PL, Polakoff PP. An anterior approach to percutaneous lower cervical cordotomy. J Neurosurg 1966;25:553-60. 47. Gildenberg PL, DeVaul RA. The chronic pain patient. Evaluation and management. Basel: Karger; 1985. 48. Rosomoff HL, Green C, Silbret M, Steele R. Pain and low back rehabilitation program at the University of Miami School of Medicine. NIDA Res Monogr 1981;36:92-111. 49. Bonica JJ. Organization and function of a pain clinic. In: Bonica JJ, editor. International symposium on pain. New York: Raven Press; 1974. 50. Bonica JJ, Loeser J. Management of pain. Philadelphia, PA: Lea & Febiger; 1990. 51. Loeser JD. Disability, pain, and suffering. Clin Neurosurg 1989;35:398-408.

2 History of the Stereotactic Societies P. L. Gildenberg . J. K. Krauss

The field of human stereotactic neurosurgery was born in 1947 when Spiegel and Wycis (> Figure 2-1) published their groundbreaking manuscript in Science [1]. In this article they describe their device, which was actually a animal apparatus suspended on the patient’s head with a plaster cap. The original Horsley-Clarke animal stereotaxic (which was the original spelling) apparatus that had been used in the laboratory was aligned with the skull by means of earplugs and orbital tabs, and the target was defined by its relationship to those bony landmarks [2]. However, there was too much variability between the boney landmarks and the human brain to use this system clinically. It was only possible when intraoperative encephalographic x-rays became available in the 1940s, that it became possible to align the human apparatus with internal cerebral landmarks. Because their human system was based on encephalographic landmarks, Spiegel and Wycis termed their procedure ‘‘stereoencephalotomy.’’ During the next decade, neurosurgeons who were interested in learning this new technique visited Spiegel and Wycis in Philadelphia, and later at each other’s institutions. Since there were no commercially available stereotactic apparatus, they first had to design and build their own device when they returned home before they could use this new procedure. The pioneer stereotactic neurosurgeons exchanged information informally and personally. They met in small groups at irregular times, usually at each other’s institutions.

#

Springer-Verlag Berlin/Heidelberg 2009

The International Society for Research in Stereoencephalotomy Periodically, the growing number of stereotactic neurosurgeons met more formally. Many of the early meetings were hosted by Ernest A. Spiegel and Henry T. Wycis at Temple Medical School in Philadelphia. In 1961, at one of their meetings, they attempted to provide a more formal venue for the exchange of stereotactic information and experience and founded the first stereotactic society, which was called the International Society for Research in Stereoencephalotomy, a term that never really caught on. When only the American members met, the meeting was designated as the American Branch of the International Society for Research in Stereoencephalotomy, and when European members met as the European Branch. They met as groups at approximately two year intervals (reference). Consequently, when the International Society for Research in Stereoencephalotomy met in 1963 in Philadelphia at what was designated the First International Symposium on Stereoencephalotomy, the society was formally chartered (> Table 2-1). The Second International Symposium on Stereoencephalotomy was held in 1965, partly in Copenhagen and partly in Vienna, the latter coincident with the Meeting of the World Federation of Neurosurgical Societies (WFNS) (> Table 2-2). The Third Symposium on Stereoencephalotomy took place in 1967 in Madrid, hosted by Sixto Obrador.

36

2

History of the stereotactic societies

. Figure 2‐1 Spiegel and Wycis

. Table 2-2 Meetings of the WSSFN 1961 1965

1967 1968

1969

1970

1973

1977 . Table 2‐1 History of the Stereotactic Societies 1961 1963 1968

1970

1973

1980

International Society for Research in Stereoencephalotomy founded, Philadelphia International Society for Research in Stereoencephalotomy chartered, Philadelphia American Branch of the International Society for Research in Stereoencephalotomy founded, Atlantic City, NJ European Society for Stereotactic and Functional Neurosurgery founded, Freiburg, Germany World Society for Stereotactic and Functional Neurosurgery founded, Tokyo, Japan American Society for Stereotactic and Functional Neurosurgery founded as society affiliated with the World Society for Stereotactic and Functional Neurosurgery First Meeting of the American Society for Stereotactic and Functional Neurosurgery, Houston, TX

1981

1985

1989

1993

1997

2001

2005

2009

The first formal independent meeting of the American Branch of the International Society for Research in Stereoencephalotomy met in Atlantic City, New Jersey, in 1968. It focused mainly on Parkinson’s disease, and was the last meeting to do so, since the field became

First International Symposium on Stereoencephalotomy, Philadelphia, PA Second International Symposium on Stereoencephalotomy, Copenhagen and Vienna Third International Symposium on Stereoencephalotomy, Madrid, Spain First Meeting of the American Branch of the International Society for Research in Stereoencephalotomy, Atlantic City, NJ Fourth Symposium of the International Society for Research in Stereoencephalotomy, New York, NY Fifth Symposium of the International Society for Research in Stereoencephalotomy, Freiburg, Germany Sixth Symposium of the International Society for Research in Stereoencephalotomy Meeting of the World Society for Stereotactic and Functional Neurosurgery, Tokyo, Japan Seventh Meeting of the World Society for Stereotactic and Functional Neurosurgery, Sao˜ Paulo, Brazil Eighth Meeting of the World Society for Stereotactic and Functional Neurosurgery, Zurich, Switzerland Ninth Meeting of the World Society for Stereotactic and Functional Neurosurgery, Toronto, Canada Tenth Meeting of the World Society for Stereotactic and Functional Neurosurgery, Maebashi, Japan Eleventh Meeting of the World Society for Stereotactic and Functional Neurosurgery, Ixtapa, Mexico Twelfth Meeting of the World Society for Stereotactic and Functional Neurosurgery, Lyon, France Thirteenth Meeting of the World Society for Stereotactic and Functional Neurosurgery, Adelaide, Australia Fourteenth Meeting of the World Society for Stereotactic and Functional Neurosurgery, Rome, Italy Fifteenth Meeting of the World Society for Stereotactic and Functional Neurosurgery, Toronto, Canada

quiescent after L-dopa was introduced in 1968 [3]. Although the meetings were relatively small, advances in pain management, epilepsy, and other movement disorders were exchanged.

History of the stereotactic societies

The core of dedicated stereotactic neurosurgeons remained interested and active in the field, which led to the Fourth International Symposium on Stereoencephalotomy in 1969 in New York, along with the meeting of the World Federation of Neurosurgical Societies (WFNS). In 1970 the Fifth International Symposium on Stereoencephalotomy was held in Freiburg, Germany, hosted by Traugott Riechert, which is also recognized as the founding and the first meeting of the ESSFN. At that time [4], both the American and European branches were considered components of the International Society.

. Figure 2-2 Logo of both the WSSFN and the ASSFN

The World Society for Stereotactic and Functional Neurosurgery It was well into the early 1970s before activity began to increase once again, which led also to organizational changes. At the Sixth Symposium of the International Society for Research in Stereoencephalotomy in Tokyo in 1973, hosted by Hirotaro Narabayashi, the name of the international organization was changed to the World Society for Stereotactic and Functional Neurosurgery (WSSFN) (> Figure 2‐2). The American branch became the American Society for Stereotactic and Functional Neurosurgery (ASSFN), and the European branch became the European Society for Stereotactic and Functional Neurosurgery (ESSFN) (> Figure 2‐3). This caused an interesting dilemma. Horsley and Clarke designated their new technique as ‘‘stereotaxic,’’ as did many of the neurosurgeons involved in this new field. However, some neurosurgeons, particularly in Europe, spelled the term ‘‘stereotactic’’ [4]. There needed to be consensus on how to spell the names of these new societies.

. Figure 2-3 Logo of the ESSFN

2

37

38

2

History of the stereotactic societies

A vote was taken, and ‘‘stereotactic’’ won, even though it was a mongrel term with ‘‘stereo,’’ meaning three dimensional, derived from Greek and ‘‘tactic,’’ meaning to touch, derived from Latin. The original term ‘‘stereotaxic’’ had been derived from two Greek words, ‘‘stereo’’ and ‘‘taxic,’’ meaning an arrangement. It was felt to reflect what stereotactic surgery did to use the term ‘‘to touch’’ rather than just to observe. The first meeting of the WSSFN was actually the reorganizational meeting held in Tokyo in 1973 and hosted by Hirotoro Narabayashi. At that meeting it was decided that the WSSFN would meet each time just prior to the meeting of the World Federation of Neurological Societies (WFNS) that met every 4 years. Since the WFNS alternated the location of the meetings from one continent to another, it became customary for the WSSFN to meet somewhere near the WFNS so members might attend both meetings with a minimum of travel, but yet in a separate venue. The WSSFN met every 4 years, with the next meeting held in 1977 in Sao˜ Paulo, Brazil, hosted by Raul Marino [5]. However, advances in the field occurred ever more rapidly, so each of the continental societies met during the intervening years. Each four year cycle began with the WSSFN meeting, then the ESSFN the following year, the ASSFN the next year, and the ESSFN the next year again. With that schedule, the ESSFN Meetings were held at 2 year intervals the first and third year of the cycle, whereas the WSSFN and ASSFN each met once every 4 years. Because there was more new information than could be provided to the members every 4 years, during the past 4 years the ASSFN also began to meet at 2 year intervals coincident with the years the ESSFN meets. The atmosphere at each of the meetings has been fraternal and informal, and the gathering of international stereotacticians maintained a feeling of collegiality. A perusal of the topics at each of the meetings of the WSSFN and the ASSFN has

served as a good indicator of what basic and clinical advances were made and what procedures and technology in stereotactic and functional neurosurgery were developed. The Proceedings of each of the meetings was published as complete issues of volumes of the official journal, Stereotactic and Functional Neurosurgery from 1968 through 2001. When the Eighth Meeting of the WSSFN in Zurich in 1981 was hosted by Jean Siegfried [6], the ESSFN declared that it was a joint meeting between the ESSFN and the WSSFN, and the ESSFN was not a component society of the WSSFN, but rather an independent society. The Ninth Meeting of the WSSFN was held in Toronto in 1985, with Ronald Tasker [7] as host. The Tenth Meeting of the WSSFN was held in Maebashi, Japan, in 1989 with Chihiro Ohye [8] as host. The Eleventh Meeting of the WSSFN was held in Ixtapa, Mexico, in 1993, with Philip L. Gildenberg [9] as the host (> Figure 2‐4). The 1997 the Twelfth Meeting of the WSSFN was held in Lyon, France, with Marc Sindou [10] as the host. It was by far the largest meeting and included many European neurologists and many local neurosurgeons. Deep brain stimulation for movement disorders was advancing rapidly, as was reflected in the program. The Thirteenth Meeting of the WSSFN was held in Adelaide, Australia, in 2001, hosted by Brian Brophy, and became a memorable meeting for an unrelated event. It was during that meeting that the terrorist attack on the World Trade Center occurred in New York. In addition to concerns about being far from family, all flights to the United States were canceled, both stranding attendees from returning to the US and preventing US neurosurgeons from attending the meeting of the World Federation of Neurosurgical Societies in Sydney immediately following the WSSFN Meeting. Many of the WSSFN speakers found themselves filling in for

History of the stereotactic societies

2

. Figure 2‐4 Presidents of the WSSFN prior to 1993, when this picture was taken. Gildenberg, Nashold, Tasker, Narabayashi, Siegfried, Ohye, and Gybels

neurosurgeons who were unable to travel to speak at the WFNS in Sydney. The most recent WSSFN Meeting was held in Rome in 2005 and hosted by Mario Meglio. The 2009 meeting will be hosted by the current President, Andres Lozano, in Toronto. Additional updated information may be obtained on the WSSFN web site at www.wssfn.org. At each international symposium from 1977 to 1985, (see > Table 2‐3) the WSSFN has presented an award to an outstanding stereotactic neurosurgeon. At the presentation of the first award, it was named the Spiegel-Wycis Award, and a gold medal was made by Prof. Manuel Velasco-Suarez to be presented to Lars Leksell (> Table 2‐4). In 1981 the award was presented to Traugott Riechert. It was felt that there were too many potential recipients for only one award to be given every 4 years, so in 1985 a gold award was presented to Jean Talairach and a silver award to Manuel Velasco Suarez. Since there was little distinction between the

requirements for the gold and silver awards, two identical gold awards have been presented since 1989. In July, 2006, the WSSFN sponsored and organized for the first time an interim meeting in Shanghai, China, which was hosted by Bomin Sun from the Shanghai Jiao Tong University, Rui Jin Hospital. The meeting covered surgical treatment for movement disorders, pain, psychiatric disease, and epilepsy. Andres M. Lozano was the meeting chairman, and Drs. Benabid, Kaplit, Krauss, Schulder, Taira, Delong, Chang, Aziz, Broggi, Sun and Zhang were among those who gave the 36 plenary lectures. It was the first time that a WSSFN meeting was held on mainland Asia. The meeting coincided with a satellite symposium on functional neurosurgery in China. Overall 250 attendees from mainland China, Taiwan and Hong Kong joined WSSFN members from 15 other countries throughout the world. The event was considered a tremendous success by those who attended.

39

40

2

History of the stereotactic societies

The American Society for Stereotactic and Functional Neurosurgery

. Table 2‐3 Meetings of the ASSFN 1980

1983

1987

1991

1995

1999

2003

2006

2008

Meeting of the American Society for Stereotactic and Functional Neurosurgery, Houston, Texas Meeting of the American Society for Stereotactic and Functional Neurosurgery, Durham, North Carolina Meeting of the American Society for Stereotactic and Functional Neurosurgery Montreal, Canada Meeting of the American Society for Stereotactic and Functional Neurosurgery, Pittsburgh, PA Meeting of the American Society for Stereotactic and Functional Neurosurgery, Los Angeles, CA Meeting of the American Society for Stereotactic and Functional Neurosurgery, Snowbird, Utah Meeting of the American Society for Stereotactic and Functional Neurosurgery, New York, NY Meeting of the American Society for Stereotactic and Functional Neurosurgery, Boston, MA Meeting of the American Society for Stereotactic and Functional Neurosurgery, Vancouver, Canada

The first separate meeting of the ASSFN was held in Houston in 1980 and hosted by Philip L. Gildenberg [11]. The 27 papers included basic neurophysiology, movement disorders, epilepsy and pain. The meeting attracted an international audience, which has been the hallmark of all of both the continental and the world stereotactic society meetings. It is interesting that even at that early date, 11 papers concerned the use of the newly developing use of computers in neurosurgical guidance, both for addressing functional targets and in the new field of image-guided neurosurgery. The next independent ASSFN meeting took place in Durham, North Carolina, in 1983, with Blaine Nashold [12] as the host, as the field showed signs of increased activity and reawakening. New technology was of greatest interest, and half of the papers concerned image guidance as it impacted brain tumor management.

. Table 2‐4 Past Recipients of the Spiegel-Wycis Award Recipient

Location

Year

Lars Leksell Traugott Riechert Jean Talairach Manuel Velasco Suarez Hirataro Narabayashi Denise Albe-Fessard Ronald R. Tasker Blaine S. Nashold, Jr. Bjorn Meyerson Philip L Gildenberg Lauri V. Laitinen Chihiro Ohye Patrick Kelly Alim-Louis Benabid

Sao˜ Paolo Zurich, Switzerland Toronto, Canada Toronto, Canada Maebayashi, Japan Maebayashi, Japan Ixtapa, Mexico Ixtapa, Mexico Lyon, France Lyon, France Adelaide, Australia Adelaide, Australia Rome, Italy Rome, Italy

July, 1977 July, 1981 July, 1985 July, 1985 October, 1989 October, 1989 October, 1993 October, 1993 July, 1997 July, 1997 September, 2001 September, 2001 June, 2005 June, 2005

History of the stereotactic societies

The 1987 meeting in Montreal, which was hosted by Andre´ Olivier, was the largest ASSFN meeting up to that time. Out of the 103 papers, 14 concerned the rapidly developing field of stereotactic radiosurgery and 41 concerned the use of computers in neurosurgery. Functional neurosurgery showed signs of significant awakening, as represented by 36 presentations. The 1991 meeting in Pittsburgh was hostedby L. Dade Lunsford [13], and represented another milestone. The stereotactic surgery meeting was followed by a two day meeting on stereotactic radiosurgery, which attracted nonneurosurgical colleagues in radiation physics and radiotherapy, as well as those stereotactic neurosurgeons who were using the Gamma Knife, the only stereotactic radiosurgical system available at that time. It was at that satellite meeting that the International Society for Stereotactic Radiosurgery was formed. In addition, this large meeting involved such new fields as tissue transplantation. It was also at that meeting that Lauri Laitinen [14,15] first presented his observations on ventroposterior pallidotomy, which signaled the return of Parkinson’s disease surgery to the functional neurosurgery arena. The ASSFN meeting was held in Los Angeles and hosted by Michael Apuzzo and David Roberts in 1995 [16,17]. Half of the papers were about classical functional neurosurgical topics of movement disorders, epilepsy and pain. There were eight papers about stereotactic radiosurgery and the rest about image guided surgery and brain tumor management. The 1999 ASSFN meeting was held in Snowbird, Utah, and hosted by Peter Heilbrun and Douglas Kondziolka. Two-thirds of the 55 papers were in functional neurosurgery, with emphasis on movement disorders, epilepsy, and pain. The rest were divided among imaging and computer guidance, stereotactic radiosurgery, and brain tumors. In 2003, the ASSFN met in New York, and was hosted by Patrick Kelly. The program

2

demonstrated the increasing use of computers in stereotactic and image guided surgery. Prior to that meeting, the FDA had provided approval of chronic deep brain stimulation, and much of the data related to that was presented. The meeting in 2006 was held in Boston and hosted by G. Rees Cosgrove. There was a significant shift toward interest in functional neurosurgery, involving both DBS and extending to epilepsy surgery. The current administrative structure includes officers elected for a term of 4 years, a board of directors and five Continental Vice Presidents. During the period from 2005 – 2009 the ESSFN leadership is represented by Andres M. Lozano (Toronto, Canada) as President, Joachim K. Krauss (Hannover, Germany) as Vice-President, Takaomi Taira (Tokyo, Japan) as Secretary-Treasurer, Michael Schulder (Newark, USA) as Assistant Secretary-Treasurer, and Philip L. Gildenberg (Houston, USA) as Historian. Honorary members include Blaine Nashold, Jean Siegfried, Ronald Tasker, Chihiro Ohye and Philip L. Gildenberg. Prior to 1975, there was no formal arrangement between the ASSFN and the American Association of Neurological Surgeons (AANS), although it was customary to have a representative of stereotactic surgery on the AANS program committee. In 1975, due to the efforts of then ASSFN President John Van Buren, the ASSFN amalgamated with the AANS and became the Section for Stereotactic and Functional Neurosurgery. This arrangement put the responsibility for the program of one and later two afternoon sessions in the hands of the ASSFN officers. In addition, members of the ASSFN automatically became members of the AANS Section of Stereotactic and Functional Neurosurgery. The ASSFN treasury, however, remained independent of the AANS, which provided the opportunity for the ASSFN to hold independent meetings every 4 years. The business meeting of the ASSFN is held at the conclusion of one of the days when the

41

42

2

History of the stereotactic societies

stereotactic scientific program is held. Since 2004, the annual residents’ research award, which has been named the Gildenberg Award, has been presented at one of the Stereotactic Sections programs. In 1984, a similar administrative arrangement was made between the ASSFN and the Congress of Neurological Surgeons (CNS). The amalgamation was facilitated by the presence of the ASSFN President, George Sypert, on the CNS Board of Directors at that time. Current details of the ASSFN can be found on the web site at www.assfn.org.

The European Society for Stereotactic and Functional Neurosurgery The formation of the European Society for Stereotactic and Functional Neurosurgery (ESSFN) dates back as far as 1970 when the International Society for Research in Stereoencephalotomy met in Freiburg, Germany. The founding fathers at that time were Fritz Mundinger, Traugott Riechert and John Gillingham, and this meeting now is also considered as the founding meeting of the ESSFN. The society was registered as a taxexempted society in Freiburg, Germany, in 1971. It was founded primarily in order to represent the interests of European functional neurosurgeons and also to enhance communication and exchange between European countries. At that time, the European idea was blossoming, but it took still several years until traveling from one European country to the other was as comfortable as it is nowadays. The judicial seat of the society was moved to Toulouse, France, in 2002. Initially, the ESSFN had a relatively isolated position in the general neurosurgical community. With the rapid development of new imaging techniques and computer technology, however, stereotactic concepts and methods had a profound impact on the progress of European neurosurgery, in general. The ESSFN over the

decades thus served both the interests of those who were subspecialized in functional and stereotactic neurosurgery and those whose activities were embedded in general neurosurgery. The ESSFN has stated its principal objectives in a mission which is displayed on the ESSFN web site (www.essfn.org). Also, its Constitution and By-Laws are displayed on the web site. The logo of the ESSFN became popular during the 1990s (> Figure 2‐3). The board of officers is elected for a term of 4 years by the General Assembly which comes together during the congresses. It is supported by an Executive Committee which has representatives from 20 different European countries. During the period from 2006 – 2010 the ESSFN leadership is represented by Yves Lazorthes (Toulouse, France) as President, Giovanni Broggi (Milano, Italy) as Vice-President, Joachim K. Krauss (Hannover, Germany) as Secretary, Damianos Sakas (Athens, Greece) as Second Secretary, and Bart Nuttin (Leuven, Belgium) as Treasurer. The honorary presidents are the former ESSFN presidents F. John Gillingham, Fritz Mundinger, Gian Franco Rossi, Bjo¨rn Meyerson, Christoph B. Ostertag, David G. T. Thomas, and Andries Bosch. There are five different categories of membership: active, associate, resident, honorary and benefactor. Membership has increased steadily over the years, and in early 2008 there were more than 230 members. The majority of members come from France, Germany, Italy, Spain, The Netherlands, and the UK. There are members, however, from almost all European countries with increasing numbers in particular from Eastern European countries and Russia. Overall, the society has about 30 non-European members coming mainly from South Korea, Japan, Mexico and the United States. Since its inception in 1970, the ESSFN organized congresses at regular intervals in various locations all over Europe (> Table 2‐5). While the first meeting was still under the umbrella of the International Society for Research in

History of the stereotactic societies

2

. Table 2‐5 Congresses of the ESSFN 1970 1972 1975 1977 1979 1981 1983 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006 2008

Founding Meeting of the European Society for Stereotactic and Functional Neurosurgery, Freiburg, Germany First Congress of the European Society for Stereotactic and Functional Neurosurgery, Edinburgh, United Kingdom Second Congress of the European Society for Stereotactic and Functional Neurosurgery, Madrid, Spain Third Congress of the European Society for Stereotactic and Functional Neurosurgery, Freiburg, Germany Fourth Congress of the European Society for Stereotactic and Functional Neurosurgery, Paris, France Fifth Congress of the European Society for Stereotactic and Functional Neurosurgery, Zurich, Switzerland Sixth Congress of the European Society for Stereotactic and Functional Neurosurgery, Rome, Italy Seventh Congress of the European Society for Stereotactic and Functional Neurosurgery, Birmingham, United Kingdom Eighth Congress of the European Society for Stereotactic and Functional Neurosurgery, Budapest, Hungary Ninth Congress of the European Society for Stereotactic and Functional Neurosurgery, Marbella, Spain Tenth Congress of the European Society for Stereotactic and Functional Neurosurgery, Stockholm, Sweden Eleventh Congress of the European Society for Stereotactic and Functional Neurosurgery, Antalya, Turkey Twelfth Congress of the European Society for Stereotactic and Functional Neurosurgery, Milano, Italy Thirteenth Congress of the European Society for Stereotactic and Functional Neurosurgery, Freiburg, Germany Fourteenth Congress of the European Society for Stereotactic and Functional Neurosurgery, London, United Kingdom Fifteenth Congress of the European Society for Stereotactic and Functional Neurosurgery, Toulouse, France Sixteenth Congress of the European Society for Stereotactic and Functional Neurosurgery, Vienna, Austria Seventeenth Congress of the European Society for Stereotactic and Functional Neurosurgery, Monterux, Switzerland Eighteenth Congress of the European Society for Stereotactic and Functional Neurosurgery, Rimini, Italy

Stereoencephalotomy, the subsequent congresses were proper ESSFN congresses. The 1981 congress in Zu¨rich was considered a joint meeting of both the WSSFN and the ESSFN. While attendance was limited in the early years to those who practiced in a subspeciality frame, the scope of topics in recent years became much broader attracting also many neurosurgeons not devoted exclusively to functional neurosurgery. During the congress, awards are available for best oral presentations by young neurosurgeons and also prizes for best posters. The ESSFN also provides grants for research in stereotactic and functional neurosurgery considering both basic and clinical research. The grant recipients will report at the congresses about their results. In the years between the congresses the ESSFN administers hands-on courses which are open to ESSFN members or those who wish to apply for membership. The purpose of these courses is to provide education and training in

functional and stereotactic techniques. The first course was given in 2003 (Tolochenaz, Switzerland) on movement disorders surgery, followed by courses on pain surgery (Toulouse, France) in 2005, and on radiosurgery (Marseilles, France) in 2007. The topics for future courses will be adapted to include new horizons, but also to provide in-depth teaching about common standards. The web site has become an important medium to keep the membership posted with updated information. Application forms for membership can be downloaded from the web site. Furthermore, members are supplied with a Newsletter that is distributed about yearly detailing new developments and announcements for grants and courses. There are many close institutional and personal links between the ESSFN and the other societies for stereotactic and functional neurosurgery, in particular to the WSSFN. Nevertheless, there is no such a formal affiliation between the

43

44

2

History of the stereotactic societies

ESSFN and the WSSFN as it has been established between the ASSFN and the WSSFN. The ESSFN also communicates with the national functional neurosurgery societies which have been established in almost all European countries. In addition, a subcommittee of the ESSFN cooperates with the UEMS (Union Europeene des Medecines Specialistes) to establish more uniform guidelines and standards for stereotactic and functional neurosurgery for all European countries.

Other International Stereotactic Surgical Societies In addition to the time-honored European and American functional neurosurgery societies, there are other international societies that organize meetings to enhance regional information exchange. The Sociedad Latinoamericana de Neurocirugia Funcional y Estereotaxia (SLANFE) is active since 1998 and covers the interests of functional neurosurgeons in Latin America. The Asian Society for Stereotactic, Functional and Computer Assisted Neurosurgery (ASSFCN) convenes meetings in Asia. In addition, several countries maintain their own Society for Stereotactic and Functional Neurosurgery, in order to accommodate their junior neurosurgeons who may not speak English or have funds to travel to the international meetings, such as Japan, Korea, Argentina, and China.

References 1. Spiegel EA, Wycis HT, Marks M, et al. Stereotaxic apparatus for operations on the human brain. Science 1947;106:349-50. 2. Horsley V, Clarke RH. The structure and functions of the cerebellum examined by a new method. Brain 1908;31:45-124.

3. Cotzias GC, VanWoert MH, Schiffer LM. Aromatic amino acids and modification of parkinsonism. New Engl J Med 1967;276:374-9. 4. Gildenberg PL. ‘‘Stereotaxic’’ versus ‘‘stereotactic’’. Neurosurgery 1993;32:965-6. 5. Gildenberg PL, Marino RJ. Seventh symposium of the international society for research in stereoencephalotomy. Conf Neurol 1978;41:1-250. 6. Gildenberg PL, Siegfried J, Gybels J, et al. Eighth meeting of the world society and the fifth meeting of the european society for stereotactic and functional neurosurgery. Appl Neurophysiol 1982;45:1-554. 7. Tasker RR, Turnbull IM, Gildenberg PL, Franklin PO, editors. Proceedings of the ninth meeting of the world society for stereotactic and functional neurosurgery. Appl Neurophysiol 1985;48(1–6):1‐498. 8. Ohye C, Gildenberg PL, Franklin PO. Proceedings of the tenth meeting of the world society for stereotactic and functional neurosurgery. Stereotac Funct Neurosurg 1990;54–55:1-564. 9. Gildenberg PL, Franklin PO, Escobedo FR, et al. Proceedings of the eleventh meeting of the world society for stereotactic and functional neurosurgery. Stereotac Funct Neurosurg 1994;63:1-301. 10. Sindou M, Martens F, Gildenberg PL, et al. Proceedings of the twelfth meeting of the world society for stereotactic and functional neurosurgery. Stereotac Funct Neurosurg 1997;68:1-318. 11. Gildenberg PL. Proceedings of the meeting of the American society for stereotactic and functional neurosurgery. Appl Neurophysiol 1980;43:89-266. 12. Nashold BS Jr, Gildenberg PL, Franklin PO. Proceedings of the American society for stereotactic and functional neurosurgery. Appl Neurophysiol 1983;46:1-252. 13. Lunsford LD, Gildenberg PL, Franklin PO. Proceedings of the meeting of the American society for stereotactic and functional neurosurgery, Part I. Stereotac Funct Neurosurg 1991;58:1-208. 14. Laitinen LV, Bergenheim AT, Hariz MI. Leksell’s posteroventral pallidotomy in the treatment of Parkinson’s disease. J Neurosurg 1992;76:53-61. 15. Laitinen LV, Bergenheim AT, Hariz MI. Ventroposterolateral pallidotomy can abolish all parkinsonian symptoms. Stereotact Funct Neurosurg 1992;58:14-21. 16. Roberts DW, Apuzzo MLJ, Gildenberg PL, et al. Proceedings of the meeting of the American society for stereotactic and functional neurosurgery, Part I. Stereotac Funct Neurosurg 1995;65:1-207. 17. Roberts DW, Apuzzo MLJ, Gildenberg PL, et al. Proceedings of the meeting of the American society for stereotactic and functional neurosurgery, Part II. Stereotac Funct Neurosurg 1996;66:1-156.

21 Angiography, MRA in Image Guided Neurosurgery P. Jabbour . S. Tjoumakaris . R. Rosenwasser

Introduction

Indication

Image-guided neurosurgery has become a standard practice in the last decade. This technology can assist the surgeon in different steps, including planning and executing the surgical procedure. So far advances in image guided surgery had little influence on vascular neurosurgery because of technical difficulties transferring 3-D vessels imaging to the neuronavigation system. The introduction of the 3-D rotational angiography has revolutionized the way we visualize and treat brain aneurysms. Sometimes it can be challenging to try to compare these views with the intraoperative microscopic view that the surgeon has. Incorporating the images of 3-D angiography in the image guided system during real time surgery is a recent technological innovation that enables the surgeon to navigate using 3-D angiogram pictures. Another innovation is fusing MRA or CTA images to the neuronavigation technique. These new techniques can be used for aneurysm, AVM and tumor surgery. One of the concerns for the neurosurgeon during tumor surgery is to avoid injury of blood vessels surrounding the tumor or encased by the tumor. Tumor surgery may be performed more safely using the intraopeartive navigated 3-D ultrasound angiography. The classical technique involves using an intraoperative ultrasound to correct the shift during surgery to keep the neuronavigation accurate. The same equipment has also Doppler capability with power Doppler to visualize vessels.

Angiography, CTA or MRA coupled to the image guided techniques is a new addition to the armamentarium for the surgical treatment of vascular lesions and tumors in the proximity of big vessels. It is essential to define exactly the 3-D relationship of the neck of an aneurysm with the surrounding vascular branches and perforating vessels in aneurysm surgery, or the exact drainage and feeding pattern of a complex arteriovenous malformation, or the exact relationship of a tumor with the surrounding vessels and its pattern of vascular invasion. All this makes this new technique essential in the surgical treatment of complex brain aneurysms, as well as distal aneurysms like pericallosal aneurysms or distal middle cerebral artery (MCA) aneurysm because it is sometimes challenging to anatomically locate these aneurysms due to the lack of big parent vessels close by. It is also used in the treatment of complex AVMs and it helps in identifying feeding and draining vessels and provides a better understanding of the AVM architecture and facilitates its resection. And finally it is also a useful technique in the surgical resection of skull base tumors located close to big vessels.

#

Springer-Verlag Berlin/Heidelberg 2009

Techniques CTA and Neuronavigation A multislice thin cuts CT is performed with superficial fiducials on the skin with intravenous

300

21

Angiography, MRA in image guided neurosurgery

contrast injection. The data obtained is transferred directly or with a compact disc to the navigation station. A pre surgical planning can start at the navigation station on the 3-D model of the CT angiogram with special attention to the lesion and the surrounding vessels and structure. During surgery the 3-D vessel model is displayed on the navigation screen, and the screen display is matched with the intraoperative microscopic view of the surgeon to try to optimize the microdissection, for skull base pathology the bone can be substracted from the image displayed by the navigation system (> Figure 21-1). Chibbaro et al. [1] reported their experience using this technique, and they concluded that this technique can provide many advantages like a quick processing time of the raw data from the CT, a better understanding of the real position of the aneurysm with respect to the surgical position of the patient, it is also helpful in tailoring the craniotomy in case of small AVMs, sparing eloquent brain and fusing functional MRI with it, and they concluded that this technique avoids major problems, such as premature bleeding and or ischemic complications which often occur due to insufficient anatomical understanding of complex vascular lesions. Kim et al. [2], described their experience using the non formatted CTA coupled to neuronavigation in the clipping of 12 distal Anterior cerebral artery aneurysms (ACA) aneurysms, they concluded that this technique enables neurosurgeons to identify a distal ACA aneurysm and facilitates the safe exposure and clipping of the aneurysm. Rohde et al. [3,4] used the term ‘‘advanced neuronavigation.’’ They coupled the 3-D CTA images, MRA images and tractography to the neuronavigation system, they reported their series of 16 patients where they used this technique during surgery. Nine skull base meningiomas, one craniopharyngioma, one epidermoid, one giant carotid artery aneurysm, two basilar aneurysms, two brain stem cavernomas. This technique

facilitated the approach in four cases contributed to a tailored approach in two cases, helped to identify hidden vessels in nine cases. Rohde [4] later on described his series of 42 aneurysms in a prospective study. They used a 3-D reformatted CTA coupled to the neuronavigation system. Twelve aneurysms of the anterior communicating artery ACOM, 17 MCA aneurysms, six internal carotid artery aneurysms (ICA), three pericallosal artery aneurysms, two vertebro basilar aneurysms, and two superior cerebellar artery (SCA) aneurysms, all ruptured with subarachnoid hemorrhage. In 24 cases the neurosurgeon used this technique to localize the aneurysm, in 18 cases it was used to understand the branching anatomy, in 8 cases to visualize hidden structures, 5 to evaluate the projection of the dome, in 2 cases to tailor the approach, the author concluded that this technique has the potential to improve the operative results by reduction of the surgical trauma and avoidance of intraoperative complications. Coenen et al. [5], used the 3-D CTA coupled to neuronavigation for the surgical treatment of small AVMs with large hematomas in four patients, this technique allows feeding arteries to be distinguished from draining veins thereby allowing the nidus of the AVM to be identified despite the presence of intracerebral blood, and decreasing surgical morbidity.

MRA and Neuronavigation Coupled to Microvascular Doppler Sonography A multislice thin cuts MRI and MRA is performed with fiducials on the skin. The images are archived on a compact disc or transferred directly to the image guidance station at the operating room where the surgery is being performed. The 3-D ultrasound volumes are acquired within the same coordinate system as navigation is performed, when the craniotomy is performed a 3-D ultrasound scan is

Angiography, MRA in image guided neurosurgery

21

. Figure 21-1 Digital subtraction angiography (upper left) and CT angiography (CTA) show a giant aneurysm of the right internal carotid artery (ICA) in a 71-year-old female patient, who was admitted after subarachnoid hemorrhage (Hunt/Hess grade IV). A 3-D reconstruction of the arterial vessel anatomy was created, rotated according to the surgeon’s perspective and displayed on the screen of the neuronavigational system during surgery (upper right). Additionally, the 2-D CT angiographic images were screen-displayed (lower left). For the surgeon, neuronavigation with CTA was especially helpful to tailor the extradural anterior clinoid process resection. Aneurysm clipping was successfully performed (lower right) and the patient made a good recovery despite her poor Hunt/Hess grade (with permission from Rohde et al. Advanced neuronavigation in skull base tumors and vascular lesions. Minim Invasive Neurosurg 2005;48(1):13-8)

performed before the dura is opened, the surgeon will be able to view reconstructed 2-D cross sectional images. Another 3-D ultrasound scan is obtained at the end of the resection and a comparison of the preoperative and postoperative 3-D ultrasounds

images is performed, this is mainly used in AVM surgery (> Figure 21-2). Mathiesen et al. [6] reported their experience using MRA with 3-D ultrasound angiography coupled to neuronavigation in the surgical

301

302

21

Angiography, MRA in image guided neurosurgery

. Figure 21-2 Preoperative angiograms (a–d) and MRI scans (e and f), intraoperative ultrasound navigational 3-D (g, posterior view; h, frontolateral view) and postoperative angiograms (i–l) (with permission from Mathiesen et al. Neuronavigation for arteriovenous malformation surgery by intraoperative 3-D ultrasound angiography. Neurosurgery 2007;60(4 Suppl 2):345-50; discussion 341-50

treatment of AVMs. Nine patients with AVMs were treated, five had underwent pre operative embolization, six patients had pre operative MRIs, in six patients the stereoscopic display technique was used, it is a volume rendering technique that provides a true sense of 3-D vision when using special glasses the skin signal is subtracted and the surgeon is able to look at the MRA images of the AVM, allowing him to plan his approach and could navigate using the pointer and trying to identify feeders and draining vessels. The AVMs were totally removed in all nine patients. The ultrasound images corresponded to the intraoperative findings. This technique led to a

minimum exploration into the nidus, in two cases when the surgeon thought that he had a complete resection of the AVM, the 3-D ultrasound was able to demonstrate a residual nidus, allowing the surgeon to remove the residual AVM. The author concluded that AVM surgery was facilitated by navigation based on preoperative MRA coupled to intraoperative 3-D ultrasound and 3-D reconstruction. The AVMs were well outlined with better understanding of the feeders and draining vessels (> Figure 21-3). Unsgaard et al. [7], used also this technique in nine patients, seven patients had AVMs in eloquent brain with Spetzler-Martin grade II in

Angiography, MRA in image guided neurosurgery

21

. Figure 21-3 Intraoperative photograph (a), biplanar angiogram (b), and 3-D-RA view (c) demonstrating a ruptured right middle cerebral artery aneurysm during the early phase of microsurgical preparation. The 3-D-RA view helps to identify the origin of the branching vessel and the localization of a large daughter bleb that was the site of rupture and was at high risk for intraoperative rerupture. The 3-D-RA model can also be viewed from behind for better identification of the temporal M2 branch that was covered by other temporal branches arising from the M3 and M4 segments (with permission from Raabe et al. 3-D rotational angiography guidance for aneurysm surgery. J Neurosurg. 2006;105 (3):406-11)

four patients, III in four patients and IV in one patient. The 9 AVMs had 28 feeders seen on the preoperative angiograms. Twenty-five of those feeders were clipped at the beginning of surgery based on the stereoscopic information from both 3-D MRA and ultrasound angiography. The other feeders were clipped in a later phase of the surgery, in one patient intraoperative ultrasound angiography revealed residual nidus that was immediately removed. Four of the seven patients with AVMs in an eloquent area had a temporary worsening of their neurological status, one patient had a permanent neurological deficit. One patient with a grade IV AVM had to be reoperated for a post operative hematoma due to a residual nidus. The authors concluded that navigated stereoscopic display of angiography offers a technology that can be used successfully to identify and clip AVM feeders in the initial phase of the operation.

Rotational Angiography and Neuronavigation 3-D rotational angiography is increasingly used to diagnose aneurysms and to better evaluate the branching vessels close to the aneurysm neck. A rotational 3-D angiography is performed. 3-D data is reconstructed, the images are archived on a compact disc or transferred directly through a network to the image guidance station. Conventional registration techniques can not be used without any CT or MRI, because the 3-D data contains only the region of interest of the angiogram, and no data representing surface matching with the patient. The registration is done with a technique that correlates the 3-D angiogram with the head positioning of the patient and this by using the angulation and the rotational coordinates from the angiogram images. A special reference head frame is used just before

303

304

21

Angiography, MRA in image guided neurosurgery

the rotational angiogram is performed to record the position of the head with respect to the coordinates of the angiographic system. After reconstructing the rotational angiography images and optimizing the quality of the image, 3-D data is exported and loaded in the navigation system. The same three point headframe that was used during angiography is repositioned on the patient’s head. The position of the three point headframe in relation to the 3-D angiography data is already known from the fluoroscopic reference position image obtained before the rotational angiography procedure. Raabe et al. [8], used the previous technique on a series of 16 aneurysms, the procedure was successful in all cases. Using this technique added an average of 19 min to the procedure. There was a good correspondence with the intraopeartive vascular anatomy. It was determined by the surgeon, that this technique was helpful in eight cases in predicting the exact location of the aneurysm and the branching vessels covered by clots or brain parenchyma. The authors concluded that this technique provides useful information about the anatomical relationship between the aneurysm and the parent or branching vessel it helps minimizing the exposure and improves the quality of aneurysm surgery in selected cases. Willems et al. [9], used a different registration technique, not involving a headframe. Following the 3-D rotational angiogram acquisition, a navigated pointer is used to determine the position of the fiducials relative to the 3-D rotational angiography data set. The angiography room in this case is provided with navigation capabilities. The rotational angiography is coupled to an image guidance system by using a new software module, that enables the determination of the positional relation between the imaged volume and the tracker plate on the image intensifier, the positional relationship between the patient and the tracker plate is determined after the patient undergoes imaging, the data is transferred to

the operating room to the navigation system, the fiducials position are localized with a pointer and the patient to image registration is completed. They tried this technique on a phantom and on two cases and they concluded that there is a small error using this technique, but this does not prevent them from preserving the orientation of the vascular tree, and the goal of offering a 3-D rotational angiograms mimicking the surgical view was also achieved with technique.

Limitations One of the limitations is the failure to depict small arteries, another limitation would be the accuracy of the navigation system, and the brain shift after the bone is removed, the dura is open, and the cerebrospinal fluid CSF is drained. The registration process is still experimental especially in the image guided rotational 3-D angiography.

Conclusion Image guided vascular surgery using MRA, CTA or 3-D rotational angiography is a new technique developed to help surgeons identifying the topographical relationship between the vascular lesion and the related parent and branching vessels it can help to tailor the exposure and the dissection of the vascular tree, and therefore minimize the risk of intraoperative complications. It is still a new technique and it can benefit from a lot of improvement mainly in the registration step. Further studies and technical development are needed to try to make this new technique a standardized one.

References 1. Chibbaro S, Tacconi L. Image-guided microneurosurgical management of vascular lesions using navigated computed tomography angiography. An advanced IGS technology application. Int J Med Robot 2006;2(2):161-7.

Angiography, MRA in image guided neurosurgery

2. Kim TS, Joo SP, Lee JK, et al. Neuronavigation-assisted surgery for distal anterior cerebral artery aneurysm. Minim Invasive Neurosurg 2007;50(3):140-4. 3. Rohde V, Spangenberg P, Mayfrank L, Reinges M, Gilsbach JM, Coenen VA. Advanced neuronavigation in skull base tumors and vascular lesions. Minim Invasive Neurosurg 2005;48(1):13-8. 4. Rohde V, Hans FJ, Mayfrank L, Dammert S, Gilsbach JM, Coenen VA. How useful is the 3-dimensional, surgeon’s perspective-adjusted visualisation of the vessel anatomy during aneurysm surgery? A prospective clinical trial. Neurosurg Rev 2007;30(3):209-16; discussion, 207-16. 5. Coenen VA, Dammert S, Reinges MH, Mull M, Gilsbach JM, Rohde V. Image-guided microneurosurgical management of small cerebral arteriovenous malformations: the value of navigated computed tomographic angiography. Neuroradiology 2005;47(1):66-72.

21

6. Mathiesen T, Peredo I, Edner G, et al. Neuronavigation for arteriovenous malformation surgery by intraoperative three-dimensional ultrasound angiography. Neurosurgery. 2007;60(4): Suppl 2:345-50; discussion 341-50. 7. Unsgaard G, Ommedal S, Rygh OM, Lindseth F. Operation of arteriovenous malformations assisted by stereoscopic navigation-controlled display of preoperative magnetic resonance angiography and intraoperative ultrasound angiography. Neurosurgery 2005;56 Suppl 2:281-90; discussion 281-90. 8. Raabe A, Beck J, Rohde S, Berkefeld J, Seifert V. Threedimensional rotational angiography guidance for aneurysm surgery. J Neurosurg 2006;105(3):406-11. 9. Willems PW, van Walsum T, Woerdeman PA, et al. Image-guided vascular neurosurgery based on threedimensional rotational angiography. Technical note. J Neurosurg 2007;106(3):501-6.

305

19 CT/MRI Safety in Functional Neurosurgery M. Schulder . A. Oubre´

Introduction Unique and ever-changing applications of imaging technologies have played an integral role in transforming the landscape of stereotactic and functional neurosurgery [1]. Both computer tomography (CT) and magnetic resonance imagery (MRI) continue to push forward the boundaries of image-guided neurological surgery. Despite the great benefits offered by CT and MRI, however, each technique poses certain risks to the safety of patients and, in some cases, of healthcare workers [2–4]. This chapter addresses pivotal considerations of the safe use of CT and MRI. The primary risks of CT scanning are associated with ionizing radiation and reactions to iodinated contrast media (ICM) [2,3,5] While MRI is often considered safer than CT because of the absence of ionizing radiation, MRI has raised its own set of safety issues. The use of gadolinium-based MR contrast agents (GBMCAs) has been linked with various types of adverse reactions, especially contrast-induced nephropathy in patients in advanced stages of renal disease [2]. In addition, MRI must be used with caution in patients with implanted devices [1,2].

DNA and generate free radicals. This is a safety concern because CT scanners usually deliver radiation doses that are often 100 times greater than those of conventional radiographic examinations, including chest X-rays or mammograms [3]. Scanner-based CT radiation carries a small but serious risk of causing cancer. Ionizing radiation can injure biologic material through several mechanisms, including formation of hydroxyl radicals that damage or break DNA doublestrands bases Concern over the risk of ionizing radiation for health problems, including malignancy, has reached a critical level in the current medical climate [5].

CT Scanning and Radiation Parameters The radiation dose for a specific study is determined by several scan parameters. These include the number of scans, tube current and scanning time in milliampseconds (mAs), size of the patient, axial scan range, scan pitch (the amount of overlap between adjacent CT slices), tube voltage in the kilovolt peaks (kVp), and the design features of the scanner used to deliver the dose [5].

Computed Tomography Safety of Ionizing Radiation

Estimations of CT Radiation-Related Cancer Risk

Background Computed tomography uses ionizing radiation: high-energy photons that are known to damage #

Springer-Verlag Berlin/Heidelberg 2009

Estimates of radiation-induced cancer risk are based on epidemiologic follow-up studies of atomic-bomb survivors in Japan and other large

280

19

CT/MRI safety in functional neurosurgery

population investigations. One large-scale study examined 400,000 radiation workers in the nuclear industry receiving about 20 milliSieverts (mSv) (a representative organ dose from a single CT scan for an adult). These investigations yielded a significant association between radiation dose and cancer-related mortality in persons exposed to doses between 5 and 150 mSv [3]. The estimated lifetime risk of death from cancer resulting from a single CT scan of the head is determined by adding the estimated organ-specific cancer risks. Again, these risks are derived from estimations of organ-specific data for cancer incidence or mortality in atomic-bomb survivors. A CT study with 2 or 3 series produces a radiation dose in the range of 30–90 mSv. Findings from some investigations suggest that this dose range is associated with a statistically significant increase in the risk of cancer in adults. Approximately 0.4% of all cancers in the United States may be associated with CT scanner-based radiation. Current estimates of excess radiationrelated cancer rates range between 1.5 and 2.0%. The evidence for increased risk is most compelling for children. Compared to adults, they are more radiosensitive and have a longer remaining life span during which time a radiation-induced cancer could form. The lifetime cancer mortality risk associated with a single head CT protocol in a 1-year-old child was 0.07% [3]. The methodology for estimating the longrange cancer risk from CT radiation is in dispute over bias. Some investigators claim that the linear no-threshold model in this dose range may overestimate the risk. Excess cancer rates have not been reported in humans for doses below 100 mSv, One possible reason for this is that defense mechanisms that inhibit radiocarcinogenesis may be much more effective at low doses [6,7]. Yet, other evidence reveals that exposure to CT-related radiation exceeds low-level radiation doses, instead falling within the range of medium-level exposure. This is noteworthy

because increased cancer risk is related to midlevel radiation doses [5].

Strategies for Reducing Radiation Dose Strategies for radiation dose reduction include inplane bismuth shielding, minimizing multiphase scanning, and decreasing or eliminating multiple scans with contrast material. CT settings can be optimized by decreasing tube current (often via automatic tube currentmodulation(ATCM)), using a larger pitch, and limiting the range of coverage. The automatic exposure-control option on new scanners can be adjusted to decrease the radiation dose. However, there is almost always a tradeoff between lowering the level of radiation dose and producing the highest quality images. The cost of reducing radiation dose by, for example, decreasing gantry rotation time, is an increase in image noise [5,8]. Minimizing patient exposure to radiation remains a priority for healthcare workers in radiology. In some cases, magnetic resonance imaging (MRI) may be a preferred option to CT scans [9]. In the absence of updated CT protocols that reflect current scientific thought, neuroradiologists and neurosurgeons must collaborate to identify optimal techniques for radiation dose reduction during a CT diagnostic or interventional procedure. Since current radiation risk estimates remain ambiguous, CT scans should be performed in accordance with the ‘‘ALARA’’ principle: ‘‘As low as reasonably achievable’’ [5,9]. Nowhere is this more crucial than for the pediatric population. Guidelines established for CT imaging in children recommend adjusting scan parameters for smaller size in order to achieve lower-dose scanning for specific applications. Following CT guidelines protocols for using age-adjusted, relatively lower tube currents may help to reduce the radiation dose for pediatric CT of the brain [3,5].

CT/MRI safety in functional neurosurgery

Iodinated Contrast Media (ICM) Used in Enhanced CT Scans

19

Non-ionic ICM are the preferred agents in CT enhanced scans of the head [2].

Background Indications for the use of iodinated contrast media (ICM) in stereotactic neurosurgery mainly include targeting of mass lesions for stereotactic biopsy and radiosurgery [10]. While in much of the developed world contrast– enhanced MRI has supplanted CT for these uses, CT contrast may still be needed [11]. Patients with pacemakers in general cannot safely undergo MRI, and others who are obese or claustrophobic may not tolerate the small bore and prolonged acquisition times [4]. MRI may not always be available, and in much of the world CT is by far the more common imaging modality. It therefore behooves neurosurgeons to understand potential problems associated with the use of ICM.

Types of Radiographic Iodinated Contrast Media (ICM) Contrast materials consist of ionic (high osmolar), and organic non-ionic (low osmolar) water soluble agents. The higher osmolarity (600–2,100 mOsm/kg) in solution for ionic contrast agents accounts for some of their adverse effects. By contrast, nonionic agents have approximately half the osmolality of ionic substances, making them less likely to affect the blood-brain barrier. These materials exhibit fewer side effects because they do not ionize in solution. Yet, nonionic agents possess the same degree of radiopacity as ionic contrast materials. Both high and low osmolar iodinated contrast agents are used in current medicine, although nonionic ICM are more common [2]. In clinical practice, ICM are typically classified by osmolality. Low-osmolality ICM may be subcategorized further into (1) nonionic monomers, (2) ionic dimers, and (3) nonionic dimers.

Safety Studies of Nonionic Versus Ionic Iodinated Contrast Media Large population studies have demonstrated the relatively lower risk of nonionic ICM compared with ionic ICM. Comparative data from two older large-scale studies suggested that the incidence of mild adverse reactions to contrast media was 2.5% for ionic ICM, but only 0.58% for nonionic ICM. Severe reactions were reported in 0.4% of patients administered ionic ICM and 0% for severe reactions after administration of nonionic ICM [12,13]. Katayama et al. reported that in a series of 337,647 cases, the overall risk of an adverse drug reaction associated with ICM was 12.66% for ionic ICM and 3.13% for nonionic ICM. The risk of a very severe adverse drug reaction was 0.04% for ionic ICM and 0.004% for nonionic ICM [14]. In a meta-analysis of studies published during the 1980s, Caro, et al. documented risks of mortality and severe nonfatal reactions in high-osmolality ICM compared to nonionic ICM. These investigators calculated a rate of severe adverse drug reaction of 0.157% for high-osmolality ICM and 0.031% for nonionic ICM. The rate of a fatal adverse reaction was one death in 100,000 patients for both types of ICM [15].

Adverse Reactions to Iodinated Contrast Media Background Despite their poorer safety record, high-osmolality ICM are still used in current medicine, primarily because of their lower cost. These media should be used selectively. High-osmolality ICM have an increased risk for adverse contrast reactions, and a significantly higher risk for contrast-related severe

281

282

19

CT/MRI safety in functional neurosurgery

adverse events [2]. The overall safety of lowerosmolality nonionic ICM has been well established since the 1990s, but adverse events have been reported. Mild and moderate adverse reactions are generally uncommon. Severe and even fatal adverse effects are quite rare, but may occur unpredictably in some patients. Serious reactions may be preceded by a mild or moderate prodromal phase. A ‘‘test injection’’ administered before a contrast-enhanced CT may increase the risk for severe adverse events [2]. ICM may also impair kidney function in certain patients or exacerbate pre-existing renal insufficiency in persons with compromised kidney function. Although contrast-induced nephropathy is not an adverse allergic reaction, it is a serious adverse event that may have debilitating consequences for high-risk persons undergoing iodinated contrast enhanced CT [2].

Safety Issues: Magnetic Resonance Imaging MRI-Related Management of Metal Implants and Foreign Bodies Background Increasing use of technologically advanced MR systems during the past 20 years has introduced growing safety concerns over the MRI environment itself [16]. Compared to older machines, new MRI scanners have stronger static magnetic fields, faster and stronger gradient magnetic fields, and more powerful radiofrequency transmission coils. While there is no evidence that magnetic fields produce irreversible biologic effects, under certain conditions several features of high-field MRI equipment pose serious hazards for the body and for implanted metal devices [17]. Expanding clinical applications of deep brain stimulation

(DBS), in particular, require a new set of safety measures for performing MRI examinations in patients with implanted neurostimulation devices [16–18]. Metal implants warrant special consideration because they are typically located near, or contiguous with, brain structures or cerebral vasculature. As recent descriptions of several MR-related injuries and at least two fatalities illustrate, strict adherence to updated evidence-based safety guidelines on MRI technology is essential. Failure to follow the manufacturer’s guidelines when performing MRI on patients with a specific neuromodulation or other metal implant may have devastating consequences. In one reported case, the DBS electrode was heated during an MRI scan of the lumbar spine on a patient with Parkinson’s disease. The heating produced a radiofrequency lesion that led to permanent neurological damage [19]. This single case study further underscores the importance of literally complying with safety guidelines for performing MRI in persons with metallic implants. Patients may be subjected to severe injury if healthcare workers attempt to generalize about various conditions, positioning schemes, or other scanning scenarios stipulated for one neurostimulation system during MRI scanning, and then inadvertently apply these generalizations to the operation of other systems [16–18]. The primary hazards associated with MRI equipment in conjunction with implanted devices are categorized as follows [4,16,17,20].





Risks associated with the static magnetic field (Bo), including complications such as movement of ferromagnetic objects, twisting, heating, artifacts, and device malfunction produced by the static magnetic field. Risks associated with radiofrequency field (RF) effects, including complications arising from body coils and specific absorption rate (SAR).

CT/MRI safety in functional neurosurgery

Risks Associated with Static Magnetic Field Strength Projectile Effect The projectile effect, or the disturbing movement of ferromagnetic material, is a primary complication of metallic implants that may occur during an MRI. Also known as the missile effect, it is caused by interactions between the static magnetic field and MRI systems [21]. Magnetic translational and rotational forces that are exerted on a ferromagnetic object can move or dislodge the object from its implanted position. A magnet of high field strength can rapidly pull different types of ferromagnetic objects into the MRI scanner. The patient is subsequently at risk for injury by any number of objects, ranging from internal aneurysm clips and pins in joints to oxygen canisters and wheelchairs [22,23].

Heating The greatest risk for MRI scanning in a patient with a DBS implant is MRI-related heating of metallic objects, especially DBS leads. Heating is poorly tolerated in the central nervous system. When electrically conductive materials are introduced within the magnet and touch the bore of the MRI scanner, these materials may overheat. If a conductive object comes in contact with the patient’s tissue, it may burn his skin, possibly resulting in irreversible lesions [16,18,20]. In addition, conductive loops that come in contact with tattoos and eye-liners containing iron-oxides may cause burns [20]. A neurostimulation system used for DBS can generate variable levels of heating. Which levels are most likely to occur, and what factors are most likely to cause overheating depend upon the specific type of implanted device as well as various parameters used for a given MRI procedure [16,18,23].

19

Intrinsic factors that influence heating include the static magnetic field strength of the MRI system (which determines the transmitted RF used for the device operation); the electrical characteristics and configuration of the individual system (electrode, extension, length, orientation of the IPG); lengths and routing of the extension and leads; the impedance of the wires; and wire breakage [16]. Extrinsic parameters in the heating equation include the type of RF coil used (transmit/ receive body vs. transmit/receive head RF coils); the landmarking site; geometry of the RF coil and the quantity of the DBS lead present within this coil; SAR (amount of RF energy delivered); method for calculating the SAR based on a particular MR system; and quantity of RF energy (whole-body averaged SAR) required for imaging [16]. RF burns may occur if currents are induced into electrocardiographic leads, or into monitoring cables and coils that are placed on the patient’s skin surface [16]. The safety of MRI in patients with DBS may be increased by placing concentric loops of DBS electrode around the burr hole cap, by using a headonly receive coil, and by adhering to the vendor recommendations re the maximum SAR that can be tolerated [16]. For certain implants that have undergone empirical testing, clinically significant thermal changes may occur at 3.0-T but not at 1.5-T. Yet other data indicate that in some cases a particular implant may exhibit clinically significant levels of heating in seconds at 1.5-T but not at 3.0-T. The greatest risk, therefore, appears to be linked with the rate of temperature increase rather than the thermal change per se. According to one report, most heating occurred within the first minute of the MRI procedure and reached a steady-state within 15 min [16]. As noted previously, in order to mitigate risks of excessive heating, established product safety guidelines for MR scanning in patients with metallic implants must be diligently followed.

283

284

19

CT/MRI safety in functional neurosurgery

Even then, the guidelines should be used only insofar as they apply to the magnetic field strengths that have been evaluated and specified in the guidelines. MR scanning at either stronger and/or weaker magnetic field strengths than those indicated in the manufacturer’s guidelines may cause substantial heating. Unless extreme precautionary measures are taken, inadvertent heating may arise and ultimately produce severe injury in the patient [16–18].

Contrast Administration in MRI Scans: Safety Issues Indications for the use of gadolinium based magnetic contrast agents (GBCMAs) are similar to those noted above for CT scanning.

Allergic Reactions Allergic reactions have been linked to the use of GBMCAs in persons with impaired kidney function. Gadopentetate dimeglumine and gadoteridol have elicited adverse reactions such as anaphylaxis in patients with impaired renal function. The package insert for gadopentetate dimeglumine warns that a history of asthma or other allergic respiratory condition may increase the possibility of a reaction, including serious, fatal, life-threatening, anaphylactoid, cardiovascular reactions, or other idiosyncratic reactions [4].

Gadolinium-based ContrastInduced Nephrogenic Systemic Fibrosis (NSF) More disconcerting than the risk for allergic reactions is the mounting evidence for a linkage between GBMCAs administered to kidney disease patients and an emerging disease called

nephrogenic systemic fibrosis (NSF). Nephrogenic systemic fibrosis is a rare, progressive, and potentially fatal fibrosing disorder that affects patients with pre-existing renal dysfunction. It is closely associated with the use of GBMCAs [24]. The disorder was originally called nephrogenic fibrosing dermopathy (NFD) because of its involvement with the skin [18]. NSF is characterized as a systemic disease of connective tissue that targets skeletal muscle, skin, and tendons. The condition is definitively diagnosed by clinical evaluation and a deep skin biopsy of the dermis, subcutaneous fat, and fascia. The pathology involves increased deposits of collagen in connective tissues, resulting in a thickening and hardening of the skin of the extremities [24,25]. In severe illness, joints may become immobile or deformed. In extreme cases of limited motion, some patients may be confined to a wheelchair. NSF also may cause injury to the diaphragm, esophagus, heart, lung, pulmonary vasculature, and skeletal muscles [25]. The disease tends to develop slowly, but advances rapidly in about 5% of patients. At present, there is no consistently efficacious therapy [18]. The American College of Radiology (ACR) recommends that patients at risk for NSF from dialysis or chronic kidney disease be screened before receiving GBMCAs. Glomerular Filtration Rate (GFR) should be measured in patients older than 60 with a history of renal disease, hypertension, diabetes, and/or severe hepatic disease/liver transplant/pending liver transplant. Patients with hepatic dysfunction should undergo a GFR assessment as close as possible to the time at which the GBMCA is to be administered for the MRI examination [26]. GBMCAs should be avoided in patients with GFRs less than 30 mL/min/ 1.73m2 unless absolutely necessary. Persons unaware that they have kidney dysfunction may be identified through medical history. If a definitive diagnosis of kidney status is not known, immediate serum creatinine testing may be warranted in addition to a GFR assessment [26].

CT/MRI safety in functional neurosurgery

Conclusions The evidence presented in this chapter clearly reinforces current expert consensus that safety remains a paramount issue for patients undergoing either CT or MRI scanning. Radiographic safety measures must be properly implemented and followed at the level of the institution, neurosurgical team, and individual healthcare worker. It is incumbent upon clinicians to keep informed of the most recent information generated by the professional organizations that develop practice guidelines and issue advisories, including critical periodic updates.

References 1. Ross PJ, Ashamalla H, Rafla S. Advances in stereotactic radiosurgery and stereotactic radiation therapy. Radiation Therapist 2001;10(1):57-72. 2. Segal AJ, Ellis JH, Baumgartner BR. ACR manual on contrast media. 6th ed. Reston, VA: ACR; 2008. 3. Brenner DJ, Hall EJ. Computed tomography – an increasing source of radiation exposure. N Engl J Med 2007;357 (22):2277-84. 4. Chung SM. Safety issues in magnetic resonance imaging. State of the art. J Neuro-Ophthalmol 2002;22(1):35-9. 5. Coursey CA, Frush DP. CT and radiation: what radiologists should know. Appl Radiol 2008;37(3):22-9. 6. Nagataki S. Comment on: computed tomography and radiation exposure. N Engl J Med 2007;357 (22):2277-84. N Engl J Med 2008;358(8):850‐1. 7. Tubiana M. Computed tomography and radiation exposure. N Engl J Med 2008;358(8):850; author reply 852–3. 8. Fricke BL, Donnelly LF, Frush DP, Yoshizumi T, Varchena V, Poe SA, Lucaya J. In-plane bismuth breast shields for pediatric CT: effects on radiation dose and image quality using experimental and clinical data. Am J Roentgenol 2003;180(2):407-11. 9. Semelka RC, Armao DM, Elias J, Jr, Huda W. Imaging strategies to reduce the risk of radiation in CT studies, including selective substitution with MRI. J Magn Reson Imaging 2007;25(5):900-9. 10. Bauman G, Wong E, McDermott M. Fractionated radiotherapy techniques. Neurosurg Clin N Am 2006;17 (2):99-110. 11. Valk J. The role of CT and NMRI in neurosurgical diagnosis. Neurosurg Rev 1986;9(1–2):43-7.

19

12. Wolf GL, Arenson RL, Cross AP. A prospective trial of ionic vs. nonionic contrast agents in routine clinical practice: comparison of adverse effect. Am J Roentgenol 1989;152:939-44. 13. Lasser EC, Berry CC, Talner LB, Santini LC, Lang EK, Gerber FH, Stolberg HO. Pretreatment with corticosteroids to alleviate reactions to intravenous contrast material. N Engl J Med 1987;317(14):845-9. 14. Katayama H, Yamaguchi K, Kozuka T, Takashima T, Seez P, Matsuura K. Adverse reactions to ionic and nonionic contrast media. A report from the Japanese committee on the safety of contrast media. Radiology 1990;175 (3):621-8. 15. Caro JJ, Trindade E, McGregor M. The risks of death and of severe nonfatal reactions with high- vs lowosmolality contrast media: a meta-analysis. Am J Roentgenol 1991;156(4):825-32. 16. Rezai AR, Baker K, Tkach J, Phillips M, Hrdlicka G, Sharan A, Nyenhuis J, Ruggieri P, Henderson J, Shellock FG. Is magnetic resonance imaging safe for patients with neurostimulation systems used for deep brain stimulation (DBS)? Neurosurgery 2005;57:1056-62. 17. Shellock FG, Crues JV. MR procedures: biologic effects, safety, and patient care. Radiology 2004;232(3):635-52. 18. Kanal E, Barkovich AJ, Bell C, Borgstede JP, Bradley WG, Jr, Froelich JW, Gilk T, Gimbel JR, Gosbee J, Kuhni-Kaminski E, Lester JW, Jr, Nyenhuis J, Parag Y, Schaefer DJ, Sebek-Scoumis EA, Weinreb J, Zaremba LA, Wilcox P, Lucey L, Sass N. ACR Blue Ribbon Panel on MR safety. ACR guidance document for safe MR practices: Am J Roentgenol 2007;188 (6):1447-74. 19. Henderson JM, Tkach J, Phillips M, Baker K, Shellock FG, Rezai AR. Permanent neurological deficit related to magnetic resonance imaging in a patient with implanted deep brain stimulation electrodes for Parkinson’s disease: case report. Neurosurgery 2005;57 (5):E1063. 20. Stecco A, Saponaro A, Carriero A. Patient safety issues in magnetic resonance imaging: state of the art [Article in English, Italian]. Radiol Med (Torino) 2007;112 (4):491-508. 21. Shellock F. Metallic neurosurgical implants: evaluation of magnetic field interactions, heating, and artifacts at 1.5-Tesla. J Magn Reson Imaging 2001;14 (3):295-9. 22. Joint Commission. Sentinel event MRI safety alert. Preventing accidents and injuries in the MRI suite. Issue 38, February 14, 2008. http://www.jointcommission.org/SentinelEvents/SentinelEventAlert/sea_38.htm Accessed 20 May 08. 23. Shellock FG, Crues JV. Commentary: MR safety and the American college of radiology white paper. Am J Roentgenol 2002;178:1349-52.

285

286

19

CT/MRI safety in functional neurosurgery

24. Chewning RH, Murphy KJ. Gadolinium-based contrast media and the development of nephrogenic systemic fibrosis in patients with renal insufficiency. J Vasc Interv Radiol 2007;18(3):331-3. 25. Broome DR, Girguis MS, Baron PW, Cottrell AC, Kjellin I, Kirk GA. Gadodiamide-associated nephrogenic systemic

fibrosis: why radiologists should be concerned. AJR Am J Roentgenol 2007;188(2):586-92. 26. Weinreb JC. Improving gadolinium-based contrast safety. Imaging Biz.com 2008;3(2):1-2.

18 CT/MRI Technology: Basic Principles M. I. Hariz . L. Zrinzo

Introduction Ever since the beginning of human stereotactic neurosurgery in 1947 [1], the radiological study has been an absolute prerequisite for the very existence of this surgery. Furthermore, the radiological study has always constituted an integral part of the surgical procedure itself. It was indeed the limitations of conventional radiology (plain X-ray, pneumoencephalography, ventriculography, arteriography), which for a long time did put the limits for what could be achieved with stereotactic neurosurgery. In 1973, Hounsfield published the method of computerized transverse axial scanning [2], which rendered him a Nobel Price in 1979. This method, which came to be known as computed tomography (CT), has literally revolutionized all neurosurgery including stereotactic neurosurgery. To begin with, and due to the axial views provided by this new imaging technique, CT introduced a new coordinate language, which had to be adopted by stereotactic neurosurgeons [3]: the anteroposterior direction became Y instead of the previous X, the dorso-ventral became Z instead of Y, and the lateral direction became X instead of Z. The advent of MRI further stimulated developments in functional stereotaxis by providing much improved soft tissue contrast, and possibility to image the brain in any desired plan. MRI forced the development of new stereotactic frames, compatible with this new imaging modality. At the same time, concerns were raised about possible distortions in the images due to magnetic susceptibilities and magnetic field inhomogeneities. Lately, #

Springer-Verlag Berlin/Heidelberg 2009

concern arose also about safety of MRI scanning in patients who are implanted with deep brain stimulation (DBS) devices [4,5]. A prerequisite for accurate CT/MRI-guided functional stereotactic neurosurgery is the adaptation of the scanning method and the stereotactic frame to each other. Additionally, for stereotactic MRI scanning, accounting for the eventual geometric distortions and the adaptation of the imaging sequence to the functional brain target aimed at, are of paramount importance. In this chapter the general principles for performing stereotactic CT/MRI scanning in the practice of functional neurosurgery are detailed. A brief description of various imaging protocols in relation to brain structure being targeted is presented.

General Principles Although routine CT/MRI examinations are performed for diagnostic purposes, the stereotactic CT/MRIstudyisalocalizationprocedureandrepresents a crucial step of the functional neurosurgical procedure. The localization procedure delineates and defines a deep-seated structure (nucleus, part of a nucleus, or pathway) in relation to a coordinate system such that the structure may be surgically targeted. This intracranial structure may be readily ‘‘visualized’’ on MRI, provided a suitable imaging sequence, as in the case of the subthalamic nucleus (STN) and the globus pallidus internus (GPi). The structure may also be a particular area of the brain, which has to be defined in relation to visualized ventricular landmarks as in the case of the

270

18

CT/MRI technology: basic principles

ventral intermediate nucleus (Vim) of the thalamus, which cannot be visualized as such on either the CT or the MRI scans. Hence, it is the geometrical accuracy in performing the scanning and the accuracy of definition of brain targets and/ or ventricular landmarks that are the hallmarks of a stereotactic CT/MRI study. Therefore, all possible sources of errors that may interfere with the requirements of accuracy of a stereotactic CT/ MRI study, should be accounted for, or preferably eliminated. The first issue in that respect is that of the geometry and image-compatibility of the stereotactic frame.

Stereotactic Frame The general requirement of any head-containing stereotactic system is to provide compatible, wellvisualized, artifact-free, fiducials or landmarks on every relevant CT/MRI slice of the stereotactic imaging study. Besides, the relationship of these external landmarks to the head must be constant during the whole scanning and also between imaging study and the subsequent surgery. The number of visible landmarks on each CT/MRI slice varies according to which frame system is used; however, a minimum of three is required to define a zero origin for the anteroposterior Y and lateral X coordinates on the slice. The accuracy of measuring the height Z coordinate is much increased if the stereotactic frame contains a fiducial permitting the assessment of the dorso-ventral position of the axial slice containing the brain target, independently from the accuracy of movement of the CT couch (if a CT study is performed, i.e.), and hence, without relying on the accuracy of the Scoutview. In case MRI is used, it is an advantage for minimizing the measurement error, and minimizing the distortion at the periphery of the MR image, where the fiducials of the frame are as close as possible to the head, that is, as close as possible to the intracranial structure, the coordinates of which are to be measured.

Immobilization of the Patient Unlike conventional radiography, a CT study, and even more so, an MRI study lasts for a certain amount of time. In routine CT/MRI scanning, the immobility of the head is important to avoid movement artifacts on the picture. In stereotactic CT/MRI scanning, the immobility of the head in relation to the frame, and to the gantry or head coil is absolutely mandatory because the scanning is performed usually with very thin slices and because at least one of the target coordinates, that is, the height coordinate Z, is sometimes based on the primary position of the head at the beginning of the scanning. To achieve a strict immobility of the head of the nonanesthetized patient during the stereotactic CT/MRI scanning, there is only one solution: it is to secure the head to a frame with skull screws and to fix rigidly the frame to the supporting couch. The discomfort for the patient should be kept to a minimum and the patient should be able to tolerate the frame. Nonrigid fixation using noninvasive interfaces [6–8] or fiducials [9] have also been used, but they assume comprehensive cooperation of the patient during the imaging study, unless general anesthesia is used. A careful explanation of the stereotactic imaging procedure, combined if needed with slight sedation, will contribute to motivate most patients to achieve an acceptable immobility of the head. Otherwise, and especially if the imaging study requires long acquisition time, the patient, who in most cases suffers from a movement disorder, must have general anesthesia during the scanning [10,11].

Scanning Plane and Alignment Conventional diagnostic axial CT images are most often acquired with a scanning plane parallel to Reid’s baseline, the orbito-metal line, or the skull base in general [12,13]. In stereotactic CT/MRI scanning, it is in many stereotactic

CT/MRI technology: basic principles

systems the geometry of the stereotactic frame that dictates the axial scanning plane. Since in many centers, most functional brain targets are still related to the atlas, and thus, to the anterior commissure-posterior commissure (AC–PC) line of the third ventricle, the stereotactic frame is mounted to the head in such a way that its base ring will be parallel to the average orientation of the AC–PC line. [14–16]. Some stereotactic systems that employ various N-shaped, Z-shaped, or V-shaped localizers do not require any specific alignment of the head and frame in relation to the CT gantry [17–23]. However, a dedicated software is then required to enable coordinate calculation. Frameless stereotactic techniques do not require any specific orientation of the head within the CT gantry or the MRI head coil. These methods rely completely on dedicated software that allows reformatting of the images according to AC–PC orientation and fusion between different imaging modalities.

Scan Thickness Even though an axial stereotactic CT/MRI scan containing the target does generally also provide the X and Y coordinates of that target in relation to any external reference fiducials, the dorsoventral Z coordinate is far from being easy to obtain accurately: on axial scans; the Z coordinate depends mainly on the thickness of the CT/ MRI slice. The volume of the voxel, that is, the impact of the partial volume effect on the boundaries of the brain structure, can be reduced by examining thinner slices. However, the spatial resolution of the image is known to decrease with thinner scans because thinner sections have a more unfavorable signal-to-noise ratio than thicker slices. This can be improved by increasing the degree of contrast on the image. The contrast resolution on the image can also be improved by longer scan time, which unfortunately prolongs the duration of the scanning and, in case of CT,

18

increases the radiation dose to the patient. Typically, for functional stereotactic purposes, it is recommended to perform the CT/MRI scanning with contiguous scans not thicker than 2 mm. Furthermore, should a sagittal or coronal reformatting of the axial CT image be desirable, the image resolution of such a reformatted image is greatly enhanced if the axial scanning has been performed with thin contiguous slices. However, it must be stressed that a reformatted or reconstructed CT image almost never reaches the degree of resolution of the axial one, and it does always carry an increased risk of measurement error. MRI readily allows for coronal and sagittal scans, although, in analogy with CT scanning, it is typically the axial scans that are used for target calculation, and most dedicated functional stereotactic softwares are based on evaluation of, and targeting on, axial scans. The distortion on the image is less on axial than on coronal and sagittal views. In all other aspects, the same rules apply for stereotactic MRI scanning (thickness of slices, parallelity with AC-PC plan, immobilization of head and frame, etc.) as for stereotactic CT scanning. The advantage of an MRI coronal scan is that it allows more readily to assess the depth of the target in relation to other visible structures, such as the relation of GPi to optic tract or the relation of STN to Substantia Nigra. Furthermore, MRI is exquisite, when used together with a dedicated software, to rehears the trajectory of the probe from cortex to target, and to allow a virtual ‘‘dry-run’’ through the structures traversed by the probe on its way to the target. Finally, on postoperative stereotactic images, MRI allows very precise evaluation of the location of DBS electrode contacts in relation to targeted structure and its surroundings, provided thin scans are obtained. It must be kept in mind that eventual geometrical distortions on MRI, which are due to the ‘‘potato ship’’ effect at the periphery of the image, are less—all other parameters equal—when the fiducials of the stereotactic frame are as close as possible to the head such as

271

272

18

CT/MRI technology: basic principles

is always the case when using the Laitinen system [24] and quite often the case—depending on the size of the head—with the Leksell system.

Measurements and Calculations For details concerning the various methods to calculate target coordinates proper to each stereotactic system, it is referred to the chapters of this book describing the respective systems. Generally speaking, there are three ways to perform measurements and calculations of the CT/ MRI coordinates of a brain target: One may use either manual measurements on enlarged hard copies, eventually with the help of matching mm-grids, or the inbuilt software of the scanner, or a specifically inbuilt or separately provided software dedicated to stereotactic measurements of a specific system. In some stereotactic systems, all three ways may be available in conjunction. However, it must be kept in mind that although a given CT/MRI machine is proven reliable as far as calibrations, accuracy, and software properties are concerned, and although a given stereotactic frame is proven mechanically accurate and CT/MRI-compatible with minimal image artifacts, the combination of the two during a stereotactic scanning on a ‘‘real’’ patient may result in measurement errors greater than what would be attributable to either of them separately. In 1992, Maciunas published an extensive application accuracy evaluation of the four most commonly used stereotactic frame systems [25]. The study was done on test phantoms scanned stereotactically with a modern CT machine with slice thicknesses from 8 mm down to 1 mm. Even with the 1-mm thick scanning, a mean target error of between 1 and 1.9 mm and a maximal error between 3.1 and 5.0 mm, dependent on the frame used, were obtained! The errors were considered greater than the mechanical accuracy of the frames and greater than the error attributable to the imaging procedure.

Clinical Applications in Functional Stereotaxis A substantial proportion of stereotactic CT/MRI studies is performed in view of a functional stereotactic procedure, that is, a stereotactic surgery for pain, movement disorder, or psychiatric disorder, where an ablative lesion or an implantation of a chronic electrode will be made in an anatomically ‘‘normal’’ structure of the brain. In these cases, the specific sub-nuclei to be targeted may not be readily seen on the CT/MRI image, and their position has to be determined in relation to visible internal reference structures, most commonly the AC-PC line.

CT Scanning for Functional Stereotaxis Computed tomography is both user- and patientfriendly. In CT-guided functional stereotaxis, the brain target cannot be visualized as such even by the most sophisticated CT scanner. Instead, the anatomical position of these structures is always defined in relation to ventricular landmarks, as has been the case during conventional ventriculography. Whereas ventriculography provides lateral and anteroposterior views of the third ventricle, CT provides an axial view. Therefore, the stereotactic CT scanning should be done not only with thin scans, but also the scanning plane should be as parallel as possible to the AC-PC line. One main difficulty has been that the ACPC line does not readily ‘‘show up’’ on the CT Scoutview. Both its exact position within the brain and its inclination in relation to any bony landmarks are subject to individual variations [26]. It has been suggested that the scanning plane which is the most ‘‘parallel’’ to the AC-PC line would be the Glabella-inion plane [27,28]. The Twining line, i.e., a line between the tuberculum sellae and the protuberantia occipitalis interna has also been advocated [29,30]. Using these bony landmarks,

CT/MRI technology: basic principles

an initial scanning of the area of the third ventricle is performed, and if it appears that the AC and PC are visualized on different slices, the gantry of the CT machine is re-angulated accordingly, and the scanning partly repeated. This technique may be time consuming and is only possible when gantryindependent CT-localizers are used. However, this technique has become rather obsolete with the advent of independent dedicated imaging softwares enabling reformatting of CT scans into axial images parallel to the AC-PC line. In other methods in which the parallelity of the scanning plane and AC-PC line can be averaged thanks to a special design of the used frame, a superimposition of the CT slice containing one of the commissures on the CT slice containing the other commissure may be sufficient to measure the length and define the level of the AC–PC line, and to assess its inclination in relation to the stereotactic frame [24,31]. This presupposes that the nonparallelity between the plane of scanning and the plane of the AC-PC line is not too exaggerated. One of the major pitfalls of stereotactic CT scanning for functional stereotactic procedures is the uncertainty in determining the height Z coordinate of the brain target. This uncertainty is not only due to the thickness of the CT slice, to eventual movement inaccuracies of the CT couch, to the geometry of the actual stereotactic frame, and/or to the nonparallelity between scanning plane and plane of AC-PC line, as has been discussed previously. The source of error in defining a functional brain target coordinate may also lie in the uncertainty in defining on CT the ventricular commissures in relation to which this very brain target is to be defined. Spiegel et al. had shown already in 1952 that the dorso-ventral thickness of the AC ranged from 1.5 to 4 mm with a mean of 3 mm [32]. Therefore, even if the CT scanning is performed with contiguous 1.5-mm thin slices, there may still be a risk of error in determining the dorso-ventral position of the AC. This risk of error is theoretically the same for the determination of the PC. Since the

18

height level of the brain target is defined in relation to the height level of the line joining the AC and PC, a repercussion of these errors on the target coordinates in the sagittal plane would ensue. Therefore some authors still prefer to perform ventriculography in addition to a stereotactic CT study (and even in addition to MRI) for the determination of a functional brain target [33–36]. Others do indeed rely solely on the stereotactic CT study and define consequently and always the AC on the CT slice lying 4 mm below the one depicting the ventral-most part of the foramen of Monro, and the PC on the slice immediately above the one showing the beginning of the aqueduct [6,24,37].

MRI Scanning for Functional Stereotaxis General Requirements Two aspects have to be considered for an MR image to be suitable as a source for direct determination of coordinates in functional neurosurgery: First, its ability to provide a good discrimination of the brain structures to be targeted, thus allowing the images to act as the patient’s individualized atlas; and second, the geometrical accuracy of the MR images has to be validated. General requirements to perform stereotactic imaging may include the following: (1) an MRI compatible stereotactic frame than can be attached to the head support of the head coil MRI; (2) a localizer with fiducials as close as possible to the head; (3) an MRI sequence adapted to the brain structure being targeted; (4) a field of view that fits the stereotactic frame; (5) a slice thickness allowing good compromise between resolution and signal-noise-ratio: with current technology, 1.5–2.0 mm slice thickness is a good compromise; (6) the pixel size in the axial plane (x, y) has to be isometric, i.e., based on a square matrix; (7) enough slices to cover with good margins the whole brain target

273

274

18

CT/MRI technology: basic principles

area, without gap between slices, and without overlapping slices; (8) the use of a transmitter– receiver head coil to ensure maximal signal, and to ensure safe postoperative imaging in patients with DBS implants; (9) regular checks of the gradient fields to minimize distortions; (10) avoiding patient movements during scanning. With few exceptions [34–36], most functional stereotactic surgeons today do use a stereotactic MRI study to determine target coordinates; however, it seems that many workers still relate the target to its atlas-defined position in relation to visualized ventricular landmarks on the MRI study. This approach ignores the main advantage of MRI: unlike ventriculography and CTscanning, MRI is not a homogeneous imaging method. Depending on the parameters of imaging, MRI studies can visualize differently and unequally well, various structures in the brain.

Thalamic Subnuclei The only commonly used brain targets in functional stereotactic neurosurgery, which still cannot be visualized as such on stereotactic thin slice MRI, are the subnulei of the thalamus. Stereotactic MRI cannot convincingly visualize several thalamic targets used in the treatment of a range of functional brain disorders: the ventroinetermediate (Vim) nucleus, targeted for treatment of tremor, the ventral oral posterior (Vop) and ventral oral anterior (Voa) nuclei, targeted, although rarely, in the treatment of dystonia and Parkinson’s, the ventroposterolateral (Vpl) and ventroposteromedial (Vpm) targeted for treatment of chronic pain, the centre median, -parafascicular (CMpf) nuclei, and ventral oral internus (Voi) targeted for the treatment of Tourette disorder. All these thalamic targets still have to be defined based on atlas coordinates in relation to AC– PC. Nonetheless, MRI, especially a T2-weighted MRI sequence can delineate the thalamo-capsular border, making it easier to determine at least the laterality of the Vim/Vop/Voa targets.

Posteroventral Pallidum The subdivisions of the globus pallidus (Globus pallidus pars interna, GPi, laminae medullaris interna and externa, Globus pallidus pars externa, GPe) and their surrounding structures (putamen, internal capsule, optic tract) can be visualized stereotactically on thin slice axial and coronal MRI using various sequences. One such sequence [38] is a nonvolumetric proton density sequence (TR/ TE 4000/15, echo-train 7, field of view 250 mm, slice thickness 2 mm, gap 0, matrix 210  256, excitations 3, imaging time 6 min and 5 s), which depicts exquisitely the details of the pallidal area (> Figure 18-1). Another sequence that has been validated by Vayssie`re et al. in Montpellier use volumetric T1 sequences [39,40]. Other MRI scanning methods, based on inversion recovery sequences, have been described by Starr et al. [41]. In all these cases, since the target itself is readily visualized, there is no need to refer to the landmarks of the third ventricle and to an atlas to obtain the location of the target in the individual patient, especially since it has been shown that the individual target location may vary substantially between patients, and also between the two hemispheres in the same patient [38,41,42].

Subthalamic Nucleus (STN) In surgery on STN, most workers who rely on MRI for targeting this structure determine its position on T1-weighted images, in relation to third ventricle landmarks and brain atlases. The few publications reporting on the use of stereotactic MRI for direct visualization and targeting of STN describe volumetric T2 weighted sequences with a rather long acquisition time [10,11,43–45], sometimes requiring reformatting of images and/or additional T1-weighted sequences that are used for targeting, and often necessitating general anesthesia during imaging. These sequences do allow exquisite visualization

CT/MRI technology: basic principles

18

. Figure 18-1 Preoperative, 2-mm thin, axial proton density stereotactic MRI scans, in two patients: (a) patient with atrophic pallidii and enlarged putaminae and (b) patient with large pallidii

of STN. The present authors, together with others [46], implemented a nonvolumetric T2-weighted MRI sequence (TR 3000–4000, TE 80–100) allowing individual visualization of the STN with fast acquisition sequences that allow imaging without general anesthesia in most patients (between 3 min 5 s and 7 min 48 s, depending on the MRI machine) (> Figure 18-2). Here also, direct visualization will make it possible to target the center of the visualized STN at surgery, without need for an indirect localization based on the atlas and the AC–PC landmarks. In all these imaging procedures, the present authors have used the Laitinen stereotactic apparatus [24,46] or the Leksell stereotactic system [47], together with MRI machines of various makings (Siemens, Philips, General Electric), regularly calibrated and assessed for field inhomogeneities and other sources of distortion.

Postoperative Stereotactic Imaging In functional stereotactic neurosurgery, stereotactic postoperative MRI is mandatory: It will unequivocally demonstrate the exact location of the stereotactic lesion or implanted DBS electrode.

. Figure 18-2 Preoperative, 2-mm thin, axial T2 weighted stereotactic MRI scan, at a 4 mm level below the AC–PC line, showing the subthalamic nuclei

This imaging should ideally be obtained with the same sequence parameters as the preoperative one. Concern about the risks of performing an MRI study on patients with implanted DBS systems has been raised [5,48]. However, a number of safety measures can be adopted to address these concerns such as use of a transmitter–receiver head coil, and ensuring the average specific absorption rate (SAR) is no more than 0.4 W/kg [4]. Recently the group of Philip Starr in San Francisco reviewed their experience over 7 years: 405 patients with 746 implanted DBS systems were imaged using a

275

276

18

CT/MRI technology: basic principles

variety of scanning techniques and on various 1.5-Tesla MRI machines, for a total of 1,071 imaging studies. They reported no adverse event, even with a SAR of up to 3 W/kg in few patients [49]. In patients with DBS, it is an advantage if postoperative imaging is performed immediately after surgery, while the frame is still on the head. If the neuro-pacemaker has already been implanted, MR images can still be obtained provided the voltage of the pacemaker is set to zero, and the output is switched off, before the patient enters the MRI room. One should be able to assess the location of the lead within the visible target and if necessary, return the patient to the operating room to relocate the lead should it become apparent that it is misplaced. The present authors consider that a DBS implant procedure is not complete until electrode localization in the intended target is verified by means of a stereotactic MRI (> Figures 18-3– > 18-4), or a stereotactic CT with image fusion to the preoperative stereotactic images.

Conclusions Notwithstanding the imaging method used, the stereotactic CT or MRI study constitutes an integral part of the stereotactic surgical procedure. It is sometimes the most difficult part of the surgery. Taking into consideration its limits and potential errors, and the fact that a measurement or calculation error at this stage may have harmful repercussions on the results of surgery and on the patient, responsibility for the stereotactic CT/MRI study lies with the neurosurgeon. Therefore, the surgeon must be well acquainted with the scanning technique, its potential pitfalls, and with target coordinate calculation, as well as being acquainted with the stereotactic frame being used. It might be wise to keep in mind the following statement made in 1985 by Lars Leksell in a paper entitled ‘‘Stereotaxis and nuclear magnetic resonance’’ [50]: ‘‘In clinical practice brain imaging can now be divided in two parts: the diagnostic

. Figure 18-3 Postoperative, 2-mm thin, axial proton density stereotactic MRI scan, at the level of AC–PC, showing artifacts of DBS electrodes in the posteroventral pallidum

. Figure 18-4 Postoperative, 2-mm thin, axial T2 weighted stereotactic MRI scan, at a 4 mm level below the AC–PC line, showing artifacts of DBS electrodes in the subthalamic nuclei

neuroradiology and the preoperative stereotactic localization procedure. The latter is part of the therapeutic procedure. It is the surgeon’s responsibility and should be closely integrated with the operation.’’

CT/MRI technology: basic principles

References 1. Spiegel EA, Wycis HT, Marks M, Lee AJ. Stereotaxic apparatus for operations on the human brain. Science 1947;106:349-50. 2. Hounsfield GN.Computerized transverse axial scanning (tomography): Part I. Description of system. Br J Radiol 1973;46:1016-22. 3. Goerss S, Kelly PJ, Kall B, Alker GJ. A computed tomographic stereotactic adaptation system. Neurosurgery 1982;10:375-9. 4. Rezai AR, Phillips M, Baker KB, Sharan AD, Nyenhuis J, Tkach J, et al. Neurostimulation system used for deep brain stimulation (DBS): MR safety issues and implications of failing to follow safety recommendations. Invest Radiol 2004;39:300-3. 5. Henderson JM, Tkach J, Phillips M, Baker K, Shellock FG, Rezai AR. Permanent neurological deficit related to magnetic resonance imaging in a patient with implanted deep brain stimulation electrodes for Parkinson’s disease: case report. Neurosurgery 2005;57:E1063. 6. Laitinen LV, Liliequist B, Fagerlund M, Eriksson AT. An adapter for computed tomography-guided stereotaxis. Surg Neurol 1985;23:559-66. 7. Hitchcock E. Stereotactic-computerized tomography interface device. Appl Neurophysiol 1987;50:63-7. 8. Bergstro¨m M, Greitz T. Stereotaxic computed tomography. A J Roentgenol 1976;127:167-70. 9. Bjartmarz H, Rehncrona S. Comparison of accuracy and precision between frame-based and frameless stereotactic navigation for deep brain stimulation electrode implantation. Stereotact Funct Neurosurg. 2007;85:235-42. 10. Bejjani BP, Dormont D, Pidoux B, Yelnik J, Damier P, Arnulf I, Bonnet AM, et al. Bilateral subthalamic stimulation for Parkinson’s disease by using three-dimensional stereotactic magnetic resonance imaging and electrophysiological guidance. J Neurosurg 2000;92:615-25. 11. Patel NK, Heywood P, O’Sullivan K, Love S, Gill SS. MRI-directed subthalamic nucleus surgery for Parkinson’s disease. Stereotact Funct Neurosurg 2002;78:132-45. 12. Lang J, Schlehahn F, Jensen HP, Lemke J, Klinge H, Muhtaroglu U. Cranio-cerebral Topography as a Basis for Interpreting Computed Topograms. In Lanksch W, Kazner E, editors. Cranial computerized tomography. Berlin: Springer, 1976. p. 24-36. 13. Lange S, Golde G. Resolution characteristics of computerized tomography and their impact on quantitative brain diagnosis. In: Lanksch W, Kazner E, editors. Cranial computerized tomography. Berlin: Springer; 1976. p. 52-5. 14. Laitinen LV. The Laitinen system. In: Lunsford LD, editor. Modern stereotactic neurosurgery. Boston: Nijhoff M; 1988. p. 99-116. 15. Lunsford LD, Leksell D. The Leksell system. In: Lunsford LD, editor. Modern stereotactic neurosurgery. Boston: Nijhoff M; 1988. p. 27-46

18

16. Mundinger F, Birg W. The imaging-compatible riechertmundinger system. In: Lunsford LD, editor. Modern stereotactic neurosurgery. Boston: Nijhoff M; 1988. p. 13-25. 17. Goerss S, Kelly PJ, Kall B, Alker GJ. A computed tomographic stereotactic adaptation system. Neurosurgery. 1982;10:375-9. 18. Kelly PJ. Contempory stereotactic ventralis lateral thalamotomy in the treatment of parkinsonian tremor and other movement disorders. In Heilbrun MP, editor. Stereotactic neurosurgery, Vol 2: Concepts in neurosurgery. Baltimore: Williams and Wilkins; 1988. p. 133-47. 19. Heilbrun MP. Computed tomography-guided stereotactic systems. Clin Neurosurg. 1982;31:564-81. 20. Kelly PJ, Goerss SJ, Kall BA. Evolution of contemporary instrumentation for computer-assisted stereotactic surgery. Surg Neurol. 1988;30:204-15. 21. Rosenfeld JV, Barnett GH, Palmer J. Computed tomography guided stereotactic thalamotomy using the BrownRoberts-Wells system for non-Parkinsonian movement disorders. Technical note. Stereotact Funct Neurosurg. 1991;56:184-92. 22. Brown RA. A computerized tomography-computer graphics approach to stereotaxic localization. J Neurosurg. 1979;50:715-20. 23. Couldwell WT, Apuzzo MLJ. Initial experience related to the use of the Cosman-Roberts-Wells stereotactic instrument. Technical note. J Neurosurg. 1990;72:145-8. 24. Hariz MI, Laitinen LV. The Laitinen apparatus. In: Gildenberg PL and Tasker RR, editors. Textbook of stereotactic and functional neurosurgery. New York: Mc Graw Hill; 1997. p. 87-94. 25. Maciunas RJ, Galloway RL Jr, Latimer J, Cobb C, Zaccharias E, Moore A, et al. An independant application accuracy evaluation of stereotactic frame systems. Stereotact Funct Neurosurg. 1992;58:103-7. 26. Talairach J, David M, Tournoux P, Corredor H, Kvasina T. Atlas d? Anatomie Ste´re´otaxique. Paris, Masson, 1957. 27. Tokunaga A, Takase M, Otani K. The glabella-inion line as a baseline for CT scanning of the brain. Neuroradiology. 1977;14:67-71. 28. Takase M, Tokunaga A, Otani K, Hori T. Atlas of the human brain for computed tomography based on the glabella-inion line. Neuroradiology. 1977;14:73-9. 29. Ohye C, Kawashima Y, Hirato M, Wada H, Nakajima H. Stereotactic CT scan applied to stereotactic thalamotomy and biopsy. Acta Neurochir. 1984;71:55-68. 30. Spiegelmann R, Friedman WA. Rapid determination of Thalamic CT-stereotactic coordinates: A method. Acta Neurochir (Wien). 1991;110:77-81. 31. Gouda KI, Freidberg SR, Larsen CR, Baker RA, Silverman ML. Modification of the Gouda frame to allow stereotactic biopsy of the brain using the GE 8800 computed tomographic scanner. Neurosurgery. 1983;13:176-81.

277

278

18

CT/MRI technology: basic principles

32. Spiegel EA, Wycis HT, Baird HW. Studies in Stereoencephalotomy. I. Topical relationships of subcortical structures to the posterior commissure. Confin Neurol. 1952;12:121-33. 33. Fox MW, Ahlskog JE, Kelly PJ. Stereotactic ventrolateralis thalamotomy for medically refractory tremor in postlevodopa era Parkinson’s disease patients. J Neurosurg. 1991;75:723-30. 34. Pinto S, Le Bas JF, Castana L, Krack P, Pollak P, Benabid AL.Comparison of two techniques to postoperatively localize the electrode contacts used for subthalamic nucleus stimulation. Neurosurgery. 2007; Suppl 2:285-92. 35. Breit S, LeBas JF, Koudsie A, Schulz J, Benazzouz A, Pollak P, et al. Pretargeting for the implantation of stimulation electrodes into the subthalamic nucleus: a comparative study of magnetic resonance imaging and ventriculography. Neurosurgery. 2006;58 Suppl 1: ONS83-95. 36. Merello M, Cammarota A, Cerquetti D, Leiguarda RC. Mismatch between electrophysiologically defined and ventriculography based theoretical targets for posteroventral pallidotomy in Parkinson’s Disease. J Neurol Neurosurg Psychiatry. 2000;69:787-91. 37. Hariz MI, Bergenheim AT. A comparative study on ventriculographic and computed tomography-guided determinations of brain targets in functional stereotaxis. J Neurosurg. 1990;73:565-71. 38. Hirabayashi H, Tengvar M, Hariz MI: Imaging of the pallidal target. Mov Disord. 2002;17 Suppl 3: S162-6. 39. Vayssiere N, Hemm S, Zanca M, Picot MC, Bonafe A, Cif L, et al. Magnetic resonance imaging stereotactic target localization for deep brain stimulation in dystonic children. J Neurosurg. 2000;93:784-90. 40. Vayssiere N, Hemm S, Cif L, Picot MC, Diakonova N, El Fertit H, et al. Comparison of atlas- and magnetic resonance imaging–based stereotactic targeting of the globus pallidus internus in the performance of deep brain stimulation for treatment of dystonia. J Neurosurg. 2002;96:673-9.

41. Starr PA, Vitek JL, DeLong M, Bakay RAE. Magnetic resonance imaging-based stereotactic localization of the globus pallidus and subthalamic nucleus. Neurosurgery. 1999;44:303-14. 42. Vayssiere N, Gaag van der N, Cif L, Hemm S, Verdier R, Frerebeau P, et al. Deep brain stimulation for dystonia confirming a somatotopic organization in the globus pallidus internus. J Neurosurg. 2004;101:181-8. 43. Zhu XL, Hamel W, Schrader B, Weinert D, Hedderich J, Herzog J, et al. Magnetic Resonance Imaging-Based Morphometry and Landmark Correlation of Basal Ganglia Nuclei. Acta Neurochir. 2002;144 959-69. 44. Schrader B, Hamel W, Weinert D, Mehdorn HM. Documentation of electrode localization. Mov Disord. 2002;17 Suppl 3:S167-74. 45. Starr PA, Christine CW, Theodosopoulos PV, Lindsey N, Byrd D, Mosley A, et al. Implantation of deep brain stimulators into the subthalamic nucleus: technical approach and magnetic resonance imaging–verified lead locations. J Neurosurg. 2002;97:370-87. 46. Hariz MI, Krack P, Melvill R, Jorgensen JV, Hamel W, Hirabayashi H, et al. A quick, and universal method for stereotactic visualization of the subthalamic nucleus before and after implantation of deep brain stimulation electrodes. Stereotact Funct Neurosurg. 2003;80:96-101. 47. Chen CC, Pogosyan A, Zrinzo LU, Tisch S, Limousin P, Ashkan K, et al. Intra-operative recordings of local field potentials can help localize the subthalamic nucleus in Parkinson’s disease surgery. Exp Neurol. 2006;198:214-21. 48. Baker KB, Tkach JA, Phillips MD, Rezai AR. Variability in RF-induced heating of a deep brain stimulation implant across MR systems. J Magn Reson Imaging. 2006;24:1236-42. 49. Larson PS, Richardson RM, Starr PA, Martin AJ. Magnetic resonance imaging of implanted deep brain stimulators: experience in a large series. Stereotact Funct Neurosurg. 2008;86:92-100. 50. Leksell L, Leksell D, Schwebel J. Stereotaxis and nuclear magnetic resonance. J Neurol Neurosurg Psychiatry. 1985;48:14-18.

22 Diagnostic PET in Image Guided Neurosurgery B. Ballanger . T. van Eimeren . A. P. Strafella

Positron emission tomography (PET) is one of the most popular imaging techniques in current neuroscience research. Due to ongoing innovations, PET continues to flourish as an interesting diagnostic tool in clinical neurology. While some imaging techniques, such as computed tomography (CT) and magnetic resonance imaging (MRI), are able to identify structural changes in the body, PET imaging is capable of detecting areas of functional changes even prior anatomical abnormalities are observed. The PET scanner does this via the use of radiolabeled molecular probes that have different rates of uptake, depending on the type and function of tissue involved. The changing of regional blood flow in various anatomical structures (as a measure of the injected positron emitter) can be visualized and relatively quantified with a PET scan. The first section of this chapter will trace the origin of PET and describe the instruments and radiopharmaceuticals. The second section will highlight studies which have application to stereotactic and/or functional neurosurgery. Whenever applicable, the current role of functional magnetic resonance imaging (fMRI) in preoperative assessment of discrete brain functions will be covered as well.

Background What is PET? PET is a nuclear medical imaging technique first developed by Michel Ter-Pogossian, Michael E. Phelps and others (1975) at the Washington #

Springer-Verlag Berlin/Heidelberg 2009

University School of Medicine [1,2], which produces a three-dimensional image of functional processes in the body with excellent sensitivity and moderate anatomic resolution (4–7 mm). PET may be used to investigate subjects in the resting state or in relationship to an event such as the occurrence of a seizure or the induction of pain. PET enables to study cerebral energy metabolism and receptor function. PET provides in vivo measurements of injected biologically active substances that have been radioactively labeled (radioligands or tracers). These radionuclides are incorporated into compounds normally used by the body such as glucose or water and then injected into the body to trace where they become distributed. Such labeled compounds are known as radiotracers. To conduct the scan, a short-lived radioactive tracer isotope is injected into the body. The radioligand decays by emitting a positron. Then the positron encounters and annihilates with an electron, producing two 511 keV gamma photons radiating at 180
from each other. PET scanners have detectors placed on opposite sides of the region from where the photons are emitted (within the patient), and the detectors register an event only if both detectors record the photon emission at the same time. As the photons are always emitted 180
from each other, this serves to both localize and quantify these events, and hence register the amount of metabolic activity. The technique depends on simultaneous or coincident detection of the pair of photons; photons which do not arrive in pairs (i.e., within a few nanoseconds) are ignored. This provides PET with a unique ability to detect and quantify

308

22

Diagnostic PET in image guided neurosurgery

physiologic and receptor processes in the body, especially in the cancer cells, that is not possible by any other imaging technique. The data collected by the PET scanner is mathematically reconstructed to produce tomographic images of tissue radioactivity concentration. Glucose is the main substrate for energy supply of the brain by oxidation. In fact, brain cells use glucose as fuel, and the more active the brain cells are, the more they will consume radioactive glucose. Using an imaging tracer that is like glucose, the PET scan is able to quantify the activity of brain tissue. Areas of less activity will use less energy, and areas with increased activity will use more energy.

Radiopharmaceuticals The key to molecular imaging in nuclear medicine is radiotracers. Radiotracers allow in vivo evaluation of different functions in the brain, namely cerebral blood flow, glucose metabolism, protein synthesis, neurotransmission, and neuroreceptor density. The application mainly depends on their chemical properties.

The standard tracer for measurement of the cerebral metabolic rate of glucose is 18F-2-fluoro-2deoxy-D-glucose (18F-FDG) [6], a sugar, for which the acquisition period is typically an hour. FDG is transported into tissue and phosphorylated to FDG phosphate, like glucose, but does not undergo significant further metabolism. Thus, it accumulates in brain in proportion to local cerebral metabolic rate of glucose. Although FDG-PET is a very powerful diagnostic tool because it gives a comprehensive image of synaptic function, it lacks specificity with regard to individual transmitter systems. There are neurodegenerative diseases involving specific neurotransmitters that do not have a distinct appearance on FDG-PET scans, probably because the cells synthesizing and releasing these transmitters are too few or too dispersed to have a local impact on energy consumption. The most evident example is Parkinson’s disease (PD), where the substantia nigra pars compacta with its profound degeneration of dopaminergic neurons is too small and metabolically too similar to the rest of the midbrain to be easily recognized in FDG-PET scans.

Specific Neurotransmitter System Unspecific Brain Activity Water

H2O15 radioactive water is administrated by bolus intravenous injection to obtain blood flow images, with a data acquisition time of about 2 min. Injections and data acquisition can be repeated at intervals equals or superior to five times the radioactive half-live of 15O (10 min). This technique is well adapted for comparing a ‘‘resting’’ condition with a condition of sensory, motor or cognitive activation. In activated brain regions, the increase in regional cerebral blood flow (rCBF) leads to a local increase in the tissue radioactive water content detected [3–5]. Glucose

In these instances, we need tracers that image specifically that particular neurotransmitter system. Several radiotracers have been developed for PET that are ligands for specific neuroreceptor subtypes (e.g., dopamine D2, serotonin 5-HT1A, etc.), transporters (e.g., [11C]McN5652, [11C] DASB, [11C]MP), or enzyme substrates (e.g., 6-FDopa). The development of PET radiolabeled receptor ligands for brain imaging holds great promise for improved specificity and sensitivity in cerebral functional imaging. Dopaminergic System

To investigate the function and integrity of presynaptic dopaminergic terminals, the most widely used tracer is the 18F-Fluorodopa (FDopa). This tracer is a substrate to DOPA decarboxylase

Diagnostic PET in image guided neurosurgery

which is expressed in abundance by dopaminergic neurons. The product, 18F-fluorodopamine, accumulates in proportion to decarboxylase activity which in turn reflects the amount of viable dopaminergic cells. Therefore, the amount of radioactivity resulting from 18F-FDopa in a region-of-interest (ROI) will reflect the number of functionally intact dopaminergic neurons within this particular region, as well as presynaptic dopamine uptake, decarboxylation to dopamine and storage [7]. The adequate modeling and interpretation of data from FDopa PET studies are far from simple and different techniques have been developed, e.g., the calculation of the influx constant Ki according to Patlak for the quantification of FDopa accumulation in the striatum [8,9]. Postsynaptically, dopamine exerts actions through several subtypes of the dopamine receptor. The dopamine receptor family consists of 5 subtypes D1-D5. In order to investigate the role of each receptor subtype, selective and high-affinity PET radioligands are required. For the dopamine D1-subtype the most commonly used ligand is [11C]-Schering 23390 ([11C]SCH) or [11C]-NNC 112, whereas for the D2/D3subtype [11C]-raclopride is a common tracer [10,11]. [18F]-fallypride is a suitable PET tracer for the investigation of extrastriatal D2 receptors [12]. For the other subtypes no suitable radioligands have been developed yet. Other tracers like [11C]-methylphenidate ([11C]MP), [11C]-dihydrotetrabenazine ([11C] DTBZ), provide complementary information on the integrity of the dopaminergic system. Methylphenidate inhibits dopamine reuptake and enhances synaptic dopamine levels. One of its isomers, dl-threo-methylphenidate has been labeled with Carbon-11 for PET [13]. Its binding in the human brain is reversible, highly reproducible and saturable and thus [11C]MP is deemed an appropriate PET ligand to measure dopamine transporter (DAT) availability [14]. The dopamine transporter (DAT) is

22

located on the plasma membrane of nerve terminals in a small number of neurons in the brain especially in the striatum and nucleus accumbens, but also in the globus pallidus, cingulate cortex, olfactory tubercle, amygdala and midbrain [15]. DAT regulates the dopamine concentration in the synaptic cleft through reuptake of dopamine into presynaptic neurons; it plays a central role in the spatial and temporal buffering of the released dopamine. Accordingly, DAT provides a good site for monitoring the function and the integrity of the dopaminergic neurons. Several DAT agents have been developed for diagnosis PD and monitoring the treatment of PD patients, based on DAT antagonists such as [11C]MP [14,16], [11C]cocaine [17,18] and 18 F-2-b-carbomethoxy-3-b-(4-fluorophenyl)tropane, ([18F]CFT) [19]. [11C]DTBZ is utilized as a tracer for in vivo imaging of the vesicular monoamine transporter (VMAT2) system [20,21]. Serotoninergic System

5-Hydroxy-tryptamine (5-HT) or serotonin is a monoamine transmitter produced in brainstem raphe nuclei and released at cortical level through widely distributed ascending pathway. Serotonin function seems to be altered in many neurologic and psychiatric disorders, in particular in depression, obsessive compulsive disorders, Alzheimer’s disease (AD) and schizophrenia. Currently at least seven major serotonin receptor classes have been identified, some of them consisting of different subtypes [22]. However, the available radioligands permit the investigation of 5-HT1A and 5-HT2A receptors only. Recently, two antagonists ligands of 5-HT1A receptors have been developed for PET studies. The first one is 18F-trans-4-fluoro-N-2-[4-(2methoxyphenyl)-1-piperazinyl]ethyl]-N-(2pirydyl)cyclohexanecarboxamide known as [18F] FCWAY which presents a much higher affinity than endogenous serotonin for 5-HT1A receptors, comparable to that of the original WAY-100635 labeled with 11C [23]. The second one is the

309

310

22

Diagnostic PET in image guided neurosurgery

4-(20 -methoxyphenyl)-1-(20 -(N-20 -pirydynyl)p-18F-fluoro-benzamido)ethylpiperazine known as [18F]MPPF which has an affinity for the 5HT1A receptor close to that of endogenous serotonin [24]. Using these two ligands, a high level of tracer uptake has been observed in high density in the hippocampus, amygdale, parahippocampal gyrus, hypothalamus, temporal pole, insula, anterior and posterior cingulated gyri [25]. Conversely, 5-HT2A receptors are present in all neocortical regions, with lower densities in hippocampus, basal ganglia and thalamus. The cerebellum and striatum are virtually devoid of 5-HT2A receptors. A quantization of 5-HT2A receptors has been possible with 18F-altanserin and 18F-setoperone [26,27]. These ligands are selective 5-HT2A antagonists and they show good reproducibility. The ligand [11C]MDL 100907 has previously been introduced to image the 5-HT2A receptor in human brain [28]. a-11C-methyl-L-tryptophan ([11C]AMT) is used as a PET marker of brain serotonin synthesis [29]. The a-methyl-L-tryptophan is converted to a-methylserotonin, which is not a substrate for monoamine oxidase and therefore accumulates in the brain. Cholinergic System

Acetylcholine (ACh) is synthesized in certain neurons by the enzyme choline acetyltransferase from the compounds choline and acetyl-CoA. In the synaptic cleft, the enzyme acetylcholinesterase (AChE) converts acetylcholine into the inactive metabolites choline and acetate. Nicotinic ACh receptors have been implicated in many psychiatric and neurologic diseases, including depression and cognitive and memory disorders, such as Alzheimer’s and Parkinson’s disease. Thus 11C-labeled nicotine was used to visualize and quantify nicotinic receptors in the brain. In recent years, the piperidine analogs C-11labeled N-methyl-4-piperidyl-acetate (MP4A) [30] and N-methyl-4-piperidyl-propionate [31] have been developed for in vivo imaging of cere-

bral AChE with PET [32,33]. As a substrate of AChE these tracers are hydrolyzed and accumulate depending on enzyme activity. AChE in human cortex is mainly expressed in the cholinergic axons, and to a lesser extent also in some cholinoceptive neurons. With impaired function and neurodegeneration of these cholinergic axons, the amount of cortical AChE is reduced. GABAergic and Glutamatergic System

GABA (Gamma Aminobutyric acid) is the most important inhibitory neurotransmitter. Its transmission is altered in epilepsy and other psychiatric disorders. Because the GABA receptor is abundant in the cortex and is very sensitive to damage, it represents a reliable marker of neuronal integrity. The tracer most widely used for central GABA binding sites is flumazenil (FMZ) labeled with [11C] [34]. The highest degree of binding is observed in the medial occipital cortex, followed by other cortical areas, the cerebellum, thalamus, striatum and pons with very low binding in the white matter. FMZ is a biochemical marker of epileptogenicity and neuronal loss; benzodiazepine receptor-density changes are more sensitive than 18F-FDG in detecting hippocampal sclerosis and benzodiazepine receptor studies were useful in the selection of patients for targeted surgery and for predicting outcome of these procedures [35,36]. As an antagonist of GABA, glutamate is the main excitatory neurotransmitter in the cortex, and alterations of glutamatergic neurotransmission are associated with many neurologic diseases. In the post-synaptic cell, glutamate receptors, such as the NMDA (N-methyl-D-aspartate) receptor, bind glutamate and are activated. Because of its role in synaptic plasticity, it is believed that glutamic acid is involved in cognitive functions like learning and memory in the brain. The tracers used to study this system ([11C]MK 801, [11C]-ketamine, [18F]-fluoroethyl-TCP and [18F]-memantine) have only

Diagnostic PET in image guided neurosurgery

a low specificity to the NMDA receptor, and relevance for clinical studies has not been established [37].

Limits of PET Radionuclides used in PET scanning are typically isotopes with short half lives such as 11C (20 min), 13N (10 min), 15O (2 min), and 18 F (110 min). Due to their short half lives, the use of PET is limited by the need for an on-site cyclotron. Therefore, PET differs from other imaging techniques in requiring more expensive equipment and highly specialized personnel, not only for scanning but also for production of the radiotracers. Unlike CT or MRI, few hospitals and universities are capable of maintaining such imaging systems.

Functional MRI fMRI is the use of MRI to measure the hemodynamic response related to neural activity in the brain. It is one of the most recently developed forms of neuroimaging. It can noninvasively record brain signals without risks of radiation inherent in other scanning methods, such as PET scans. It can record on a spatial resolution in the region of 3–6 mm with a relatively good temporal resolution (in the order of seconds) compared with techniques such as PET. Since neurosurgery relies on a precise delineation of the structural and functional aspects of brain, the role for fMRI in neurosurgical planning can be significant, especially when the presence of a tumor alters the expected location of a function, or when the location of the tumor is in an area with an uncertain function such as association cortices or language-related processes. An emerging group of investigators have reported fMRI results that are consistent with

22

electrophysiology, PET, cortical stimulation, and magneto-encephalography and serve to document that fMRI does provide a source of precise functional and structural information for neurosurgery [38–45]. Further, the potential role of fMRI in directing decisions about surgical and diagnostic procedures has also been demonstrated [46,47]. fMRI can be useful in the selection of patients for whom a surgical resection is attempted and could aid in the decision-making whether to operate on a patient who has been previously considered inoperable. fMRI is a useful tool in the decisional scheme of treatment of low-grade astrocytomas or arteriovenous malformations (AVM) in the rolandic area in intact or slightly impaired patients. fMRI can be repeated in selected patients with slow growing brain tumors or congenital lesions such as AVM to study cortical reorganization phenomena. In many neurosurgical centers, the Wada-test (barbiturate injection into one of the internal carotid arteries) was substituted by fMRI to determine the hemispheric dominance of language. After the dura had been opened and/or part of the tumor had been removed, the functional tissue that the surgeon wants to preserve might have shifted. As a future potential, real-time fMRI could identify this functional tissue intraoperatively, comparable to an inverse intraoperative frozen section diagnosis.

PET as a Differential Diagnostic Tool Since the development of PET, in vivo imaging has become the method of preference to assess a variety of neurodegenerative and neuropsychiatric disorders [48,49].

311

312

22

Diagnostic PET in image guided neurosurgery

Parkinson’s Disease Advances in Understanding Parkinson’s Disease In the last two decades, measurements of rCBF (with methods like PET or fMRI) as an indicator of neuronal activity have greatly advanced our understanding of the neuronal processes underlying motor and cognitive deficits in patients with idiopathic Parkinson’s disease (IPD). In initial H2O15 PET activation studies on motor planning and execution in IPD, the hypothesis of an excessive cortical inhibition from corticostriatal loops had been strengthened [50,51]. The separate contributions of dopamine loss in the striatum and direct cortical involvement in cognitive impairment in IPD had been the subject of several studies in recent years (see [52,53] for reviews). rCBF PET and fMRI have also been successfully used to investigate the functional impact of pharmacological or surgical interventions in IPD (see [54,55] for reviews). Currently, the identification of genetically defined at-risk populations yields great potential to identify adaptive neuronal mechanisms in a preclinical state of parkinsonism with neuroimaging techniques (see [55] for review).

Differentiate Between Idiopathic Parkinson’s Disease and Atypical Parkinsonism The clinical diagnosis of IPD seems fairly straightforward in most cases. Conversely, clinical pathology studies demonstrated that up to 25% of the patients clinically diagnosed with IPD had the post mortem diagnosis of progressive supranuclear palsy (PSP), multiple system atrophy (MSA), vascular parkinsonism or AD [56]. Yet, establishment of an early and accurate diagnosis impacts on management, helps to avoid inappropriate treatment and assists in the

evaluation of novel drugs. A wide range of objective neuroimaging methods currently contribute to establish diagnosis. Especially functional imaging techniques like PET and single photon emission computed tomography (SPECT) can be used with various radioligands to provide quantitative assessment of dopamine functioning in- and outside of the brain. In terms of a differential diagnostic tool, the degeneration of dopaminergic neurons with reduction of their respective PET markers has been described in all diseases that cause parkinsonism, but the relative involvement of the pre- and postsynaptic metabolism in the striatum and the rostral and caudal parts of the striatum provides some distinction between diseases. PET can demonstrate the disturbance of dopamine synthesis that is the hallmark of PD. The most widely used tracer in PD is FDopa. In Parkinson’s disease, the PET scan shows a characteristic pattern of reduced striatal uptake for FDopa, and it begins to appear very early in the course of the disease [57] most strongly on the side opposite to the major motor signs [58,59] and predominantly in the posterior part of the putamen, indicating loss of more than 50% of dopaminergic neurons projecting to this part of the striatum [60]. This typical differential intrastriatal distribution of reduced uptake is often referred to as the ‘‘rostrocaudal gradient’’ [61]. Although the ability to demonstrate reductions in FDopa uptake in the putamen can help in the diagnosis of IPD, the differentiation between IPD, PSP, MSA, or corticobasal degeneration (CBD) is more difficult. It had been indicated that in PSP and MSA, nigral projections to the caudate nucleus become involved earlier in the course of disease resulting in more equally decreased FDopa uptake in terms of rostrocaudal distribution [62]. However, due to a significant overlap, FDopa PET alone seems not to be able to distinguish between different forms of parkinsonism [63]. An alternative measure of presynaptic dopamine terminal integrity is PET

Diagnostic PET in image guided neurosurgery

imaging with radiotracers that bind either to DAT ([11C]MP) or the VMAT2 ([11C]DTBZ). These methods show similar findings in IPD to those seen with FDopa PET and the ability to differentiate different forms of parkinsonism is similarly low [64]. The distinction is much better (80–90%, according to Brooks 2002 [65]) for indicators of striatal postsynaptic D2 receptors ([11C]raclopride) or glucose metabolism ([18F]FDG) [66] (see > Figure 22-1). This distinction between PSP and MSA on the one side and IPD on the other side rests mainly on the fact that in PSP and MSA, dopaminergic neurodegeneration affects both pre- and postsynaptic nerve fibers, whereas in IPD there is a presynaptic dopaminergic deficit in the striatum while postsynaptic striatal neurons are fairly intact and their D2 receptors binding and glucose metabolism have been shown to be normal or even increased in

22

untreated patients [67,68]. In contrast, striatal glucose metabolism is reduced in 80–100% of probable atypical parkinsonism patients [65]. With FDG, CBD differs from PD by a metabolic decrease in premotor, primary motor, supplementary motor, primary sensory and parietal associative cortices but also in caudate and thalamus [69]. Based on FDG or D2 receptors studies, however, distinction among MSA, PSP and CBD is barely possible, limiting the sensitivity of this investigation in the differential diagnosis of parkinsonism [65,70,71]. In many neuroimaging facilities only SPECT might be available. Generally speaking, in terms of differential diagnosis of parkinsonism, the same strengths and limitations apply to SPECT imaging of the presynaptic dopamine transporter (123I-b-CIT or 123 FP-CIT) and postsynaptic dopamine receptor (123I-IBZM).

. Figure 22-1 Representative PET images of FDOPA, RACLO and FDG at the mid-striatal level from one patient with Parkinson’s disease (PD) (top row) and one patient with multiple system atrophy (MSA) (bottom row). Each FDOPA, RACLO and FDG image is scaled relative to common maximum and background levels. At the putamen level, note the marked decrease of dopamine D2 receptor binding (RACLO) and glucose consumption (FDG) in MSA patient which cannot be found in PD patient. Reduction of putaminal DOPA influx constants are similarly visible in PD and MSA (from Antonini et al., Brain 1997;120(12):2187–95)

313

314

22

Diagnostic PET in image guided neurosurgery

Dementias Dementia is a clinical syndrome most commonly characterized by impaired short- and long-term memory and associated with deficits in many cortical functions which interfere significantly with the activities of daily life. Dementia is a common disease and prevalence continues to grow with increased human life expectancy. The most frequent cause is Alzheimer’s disease, accounting for 60–70% of all dementias in the elderly, followed by Lewy body dementia (LBD) (10–25%), vascular dementia (10–15%) and frontotemporal dementia (FTD) (5–10%). Synaptic dysfunction or loss – a hallmark of different types of dementia – entails at the molecular level several mechanisms that finally result in decreased energy demand. Therefore, assessment of glucose metabolism with FDG-PET is a valid tool for imaging the energy metabolism of the brain and its typical changes in dementia [72,73] as it can differentiate Alzheimer’s from other confounding types of dementia [74–76]. A consistent finding that has been noted since the earliest PET studies in AD is the hypometabolism affecting the temporal and parietal association cortex [77,78]. Recently, some studies using voxel-based comparison against normal reference data show that the posterior cingulate gyrus and the precuneus are also impaired early in the course [79]. In the parieto-temporal association cortices of AD patients, the reduction in glucose metabolism is greater than the reductions in blood flow and oxygen metabolism [78]. In contrast to other dementia types, glucose metabolism in the basal ganglia, primary motor and visual cortex, and cerebellum is usually well preserved [72–75]. Indeed FDG-PET in dementia with Lewy bodies reveals changes similar to those seen in AD plus additional hypometabolism in primary and associative visual cortices [80–83]. Occipital hypometabolism is the feature of DLB that discriminates it from AD. FDG-PET

scanning in FTD is associated with hypometabolism in the frontal, anterior and medial temporal cortices [84,85]. Low striatal DAT activity (e.g., indexed by [11C]MP) occurs in DLB but is normal in AD, making DAT scanning particularly useful in distinguishing between the two disorders [86]. FTD is a syndrome that can be clinically difficult to distinguish from AD, but in FTD amyloid deposition is not a characteristic pathological finding. Recently, it has been shown that N-methyl[11C]2-(40 methylaminophenyl)6-hydroxy-benzothiazole (PIB, a PET tracer with amyloid binding properties) could potentially aid in differentiating between FTD and AD [87,88] (see > Figure 22-2). The assessment of specific neurotransmitter systems with PET is likely to contribute substantially to clinical distinction between different neurodegenerative diseases that may lead to dementia. Receptor ligands for the cholinergic, dopaminergic, and serotoninergic system and newly developed tracers that label amyloid plaques are likely to play an important role. The full clinical relevance of these developments probably will turn up when more specific and also coursemodifying drugs for dementia treatment become available.

PET as a Preoperative Assessment Tool Brain Tumors Diagnosis and Staging PET has emerged as a powerful diagnostic tool in differentiating malignant from benign tumors. Indeed, the uncontrolled cellular proliferation is the hallmark of malignant transformation and offers the perfect target for diagnosis and evaluation with functional imaging. To this end, a

Diagnostic PET in image guided neurosurgery

22

. Figure 22-2 PIB standardized uptake values (SUV) of four representative subjects. FTD PIB negative: a 65-year-old patient with a clinical diagnosis of frontotemporal dementia (FTD; MMSE = 29, CT scan normal) with a PIB retention similar to healthy control. FTD PIB positive: a 75-year-old patient with a clinical diagnosis of FTD (MMSE = 27, CT scan normal) with a PIB retention similar to that found in AD patients. AD: scan of a typical patient with Alzheimer disease. SUV were obtained using the time interval 40–60 min. The results of this study indicate that the majority of FTD patients displayed no PIB retention (FTD negative) in line with the assumption that amyloid deposition is a characteristic neuropathological feature of AD, but not FTD. However, two of the ten patients with clinical diagnosis of FTD tested in this study (FTD positive) had a PIB retention similar to the AD patients suggesting that their true diagnosis might be AD. Therefore, PIB could potentially aid to differentiate between FTD and AD (from Engler et al., Eur J Nucl Med Mol Imaging 2008;35:100–6)

number of radiotracers – targeting changes in glucose metabolism (FDG), protein (e.g., [11C]methionine) or DNA (e.g., [11C]-thymidine) synthesis – have been developed to exploit these differences between malignant and normal cells. FDG-PET

Currently, the evaluation of brain tumors with FDG-PET is widely used in clinical oncology as the rate of glucose utilization is directly proportional to the degree of malignancy [89]. FDG uptake in low-grade gliomas (which are mostly grade II in adults) is usually similar to that of normal white matter, whereas most grade III anaplastic gliomas have a FDG uptake similar to or exceeding that of normal gray matter. Untreated glioblastomas, the most malignant

gliomas (grade IV), also have increased uptake of FDG, which might be heterogeneous throughout the tumor owing to the microscopic and macroscopic necroses that are typical in this tumor type [90]. Accordingly, FDG-PET is a valuable tool for accurate differentiation of lowand high-grade gliomas (> Figure 22-3). Across oncologic applications, the sensitivity and specificity of FDG-PET ranged from 84 to 87% and 88 to 93%, respectively. However, the main limitation of FDG for clinical studies of brain tumors is the high glucose consumption of normal gray matter (45 mmol/100 g/min) that may be in the same range as malignant tumors. Thus, even malignant tumors may be missed if surrounded by intact gray matter. Ac-

315

316

22

Diagnostic PET in image guided neurosurgery

. Figure 22-3 Co-registered MRI and FDG and 11C-methioinine PET images in glioblastoma. The contour delineates the areas of contrast enhancement (top row, middle) and is projected onto all other images. On the FDG images, only part of the contrast-enhancing area shows uptake comparable to normal gray matter, indicating the most aggressive part of the tumor, whereas methionine uptake exceeds the contrast enhancing area, which includes low-grade and tumor infiltration zones (from Herholz et al., Lancet Neurol 2007;6(8):711–24)

cordingly, evaluation of glucose consumption in brain tumors can only be done reliably if the location of the tumor is accurately known, best by digital image coregistration with MRI or CT. Amino Acid Uptake

Most brain tumors show an increased uptake of amino acids that is probably due to increased carrier-mediated transport at the blood–brain barrier (BBB). Increased uptake is also seen in most low-grade gliomas in the absence of BBB damage, which is a substantial advantage over CT, MRI, and FDG-PET [91–93]. Other 18 F-tagged radioisotopes (e.g., tyrosine) have also been found useful to improve diagnostic assessment of cerebral gliomas [94]. The most commonly used radiolabeled amino acid is 11C-L-Methionine (MET). Many studies have reported the use of MET to investigate malignancy, extent of tumor spread, effec-

tiveness of therapy, and prognosis of brain tumors [95–99]. Although MET PET has a limited ability to grade gliomas, it will provide reliable information about the extent of tumor infiltration.

Prognosis PET helps to assess tumor localization, extension and degree of malignancy, but histopathological examination of the tissue still is indispensable for definitive diagnosis and prognosis. Stereotactic biopsy is the least invasive way to obtain a specimen for histopathological classification of brain lesions. To this end, FDG-PET is used as stereotactic PET for directing biopsies accurately in the abnormal foci of brain tumors [100–103]. Many malignant gliomas are heterogeneous, but grad-

Diagnostic PET in image guided neurosurgery

ing needs to be done on the most malignant parts, which are commonly difficult or impossible to identify with standard structural imaging. The most metabolically active tumor part on PET (FDG or amino acid) indicates the most informative location for taking a biopsy [103–105]. Furthermore, in biopsy-proven low-grade gliomas, tumoral FDG uptake correlates well with the risk of malignant transformation [106,107].

Differentiation Between Recurrent Tumor and Radiation Necrosis Detection of recurrent tumor is an important issue because growth of recurrent tumor will lead to increase of symptoms and ultimate death of the patient. FDG-PET has been used successfully for that purpose in high-grade tumors [108], for detection of malignant progression in low-grade gliomas [109] and to distinguish radiation necrosis from recurrent tumor. Classically recurrent tumor is ‘‘hot’’ on FDG-PET studies and radiation necrosis is ‘‘cold’’; however, these two processes are often interleaved, so the reported sensitivity and specificity is quite low [110]. But there is increasing evidence that amino acid tracers can provide this discrimination [111].

Epilepsy Epilepsy is one of the most common neurological conditions. Almost 60% of patients respond to the first tried antiepileptic drug. However, 20% of people with epilepsy continue to have seizures despite adequate anti-epileptic drug treatment. This failure of drug treatment has led to an increasing interest in neurosurgery for epilepsy, particularly surgical approaches which aim to remove the ‘epileptic focus’ and, therefore offer the opportunity for these patients to be-

22

come free of seizures. One of the main objectives of presurgical investigation in patients with medically refractory epilepsy is to define the boundaries of the epileptogenic region to be resected. The epileptogenic zone refers to the region of cerebral cortex that is both necessary and sufficient to generate epileptic seizures, hence its entire removal is required for a successful outcome. Toward this goal, chronic intracranial EEG evaluation remains the gold standard. However, because this method carries a risk of morbidity and possible mortality, it is appropriate only when reliable conclusions cannot be obtained by less invasive methods. In parallel, a wide range of imaging techniques is valuable for imaging the epileptogenic zone, including highresolution T1 MRI, T2 signal quantitation, MR spectroscopy, diffusion imaging, PET, SPECT and simultaneous EEG-fMRI. MRI is often able to identify the source of seizure in patients with focal epilepsy. However, 20 to 30% of potential surgical candidates with focal epilepsy have normal MRI [112]. Interictal FDG-PET has been shown to be more sensitive than MRI in the identification of seizure of temporal lobe origin [113] and a valuable tool in patients with intractable epilepsy without a structural lesion [114–116]. The characteristic finding is a regional reduction in glucose uptake during the interictal state [117–119]. However, when investigating partial epilepsy, the benzodiazepine ligand [11C]FMZ may also be used which is a selective antagonist of GABAA– BZD receptors. The reduction of FMZ binding is much more focally restricted than reductions of FDG uptake [120] and the area of focal reduction of FMZ binding is probably also a better indicator of the epileptogenic zone that needs to be resected to become seizure free [121,122]. Therefore FMZ-PET can be more useful in preoperative planning than [18F]FDG alone. Although interictal PET provides useful information in temporal and extratemporal lobe epilepsy, its

317

318

22

Diagnostic PET in image guided neurosurgery

role is more important in patients with normal structural imaging.

Functional Brain Mapping with PET and fMRI The neurosurgeon often has to balance the benefits of brain tissue removal (e.g., in focal epilepsy or mass lesions) and the potentially devastating iatrogenic disruption of brain functions. Therefore a precise delineation of the structural and functional aspects of brain can prove very helpful in the preoperative decision making process, especially when the presence of a tumor alters the expected location of a function. Two of the most widely used approaches include PET and fMRI. Advantages of fMRI are: higher spatial and temporal resolution, more and different functional runs, shorter examination time, wider availability, longitudinal examinations, non-invasiveness and cost-effectiveness, easy registration to anatomical images. Advantages of PET are: higher signalto-noise ratio, lesser susceptibility to artifacts (motion, draining veins). Moreover, in deep brain stimulation (DBS), functional imaging has been used to investigate the impact of the procedure, but also identified potential stimulation areas.

Motor Mapping H2O15 PET and fMRI both are able to delineate brain regions activated by volitional movements, namely the primary sensorimotor cortex, the supplementary motor area, the lateral premotor cortex and the superior parietal lobule. Preoperative motor mapping with fMRI has been described [123–125] and validated against (the more invasive) electric cortical stimulation (ECS). Majos and colleagues studied 33 patients with brain tumors in the rolandic area and found an agreement of both methods of 98%

for combined motor and sensory representations [124]. Using 3T fMRI and ECS, Roessler et al. studied 22 patients with gliomas involving the primary motor cortex [125]. Motor foci were successfully detected with fMRI in all patients, but a successful intraoperative stimulation of the primary motor cortex was possible only in 77% of the patients. Moreover, in this subgroup, the motor focus in ECS and fMRI was identical within 1 cm. These results point to the direction, that motor mapping with fMRI or PET are safe and reliable techniques to assess the risk of a motor deficit following surgical procedure.

Language Mapping The lateralization of language is of special interest in patients with medial temporal lobe epilepsy and with tumors of the ventral frontal and temporal lobe. To this end, the selective intracarotid amobarbital application (Wada test) had been the gold standard for almost 50 years. Recently however, the Wada test gets more and more replaced by less invasive procedures such as fMRI. Klo¨ppel and Bu¨chel reviewed four studies comparing the Wada test with fMRI based language lateralization [126]. The authors summarize an agreement of about 90% of the two methods and note the advantage of fMRI to additionally provide a precise localization of language functions. They predicted that fMRI will be most widely used to assess language lateralization. But there might be an essential advantage of PET on the clinical application of language activation studies that challenges a predominant role of fMRI. Active speaking during language production tasks does not induce technical artifacts (as it is common with fMRI), and therefore, direct monitoring of task performance is possible even in functionally impaired subjects [127–129].

Diagnostic PET in image guided neurosurgery

Deep Brain Stimulation Pre- and post-operative imaging of H2O15 PET has been used to define the effects of deep brain stimulation in cases of Parkinson’s disease, depression and pain syndromes. For instance, concerning subthalamic nucleus (STN) stimulation in PD, three H2O15 PET studies found an enhanced movement-related activity in the dorsolateral and mesial prefrontal cortex, two areas known to be underactive in unmedicated PD [130–132]. For the treatment chronic pain syndromes, Davis and associates report on the changes on pre- and postoperative PET scanning in patients undergoing placement of thalamic stimulators. The investigators found that DBS caused activation of the contralateral anterior cingulate cortex, a known centre involved in pain and analgesia [133]. In parallel there has been some evidence that chronic electrical stimulation of the primary motor cortex (MCS) may relieve motor symptoms of PD. This surgical technique has been proposed as an alternative for selected PD patients who are considered poor candidates for DBS of the STN. However, to date the MCS technique remains a controversial procedure. Recently, using PET, our group [134] suggest that while unilateral MCS is probably a simpler and safer surgical procedure than DBS of STN, it did not improve motor performance nor significantly modify the activation pattern of movement-related rCBF in patients with advanced PD. These observations along with recent negative clinical experiences in PD patients [135] raise some controversy about the efficacy of this therapeutic modality in PD. Sometimes, functional imaging studies even identify new DBS targets. Based on the converging PET findings that the subgenual cingulate region (Brodmann area, BA, 25) is overactive in treatment resistant depression, Mayberg and colleagues tested DBS of adjacent white matter tracts to modulate BA25. They found a sustained

22

remission of depression in four of six patients. This clinical improvement was associated with a marked reduction in local cerebral blood flow as well as changes in downstream limbic and cortical sites [136]. Using PET, a possible cerebral origin of cluster headache has been visualized in the hypothalamic gray matter [137] prompting the successful use of DBS in the inferior posterior hypothalamus in intractable chronic cluster headache patients [138–140].

References 1. Phelps ME, et al. Application of annihilation coincidence detection to transaxial reconstruction tomography. J Nucl Med 1975;16(3):210-24. 2. Ter-Pogossian MM, et al. A positron-emission transaxial tomograph for nuclear imaging (PETT). Radiology 1975;114(1):89-98. 3. Posner MI, et al. Localization of cognitive operations in the human brain. Science 1988;240(4859):1627-31. 4. Fox PT, et al. Mapping human visual cortex with positron emission tomography. Nature 1986;323(6091):806-9. 5. Raichle ME, et al. Practice-related changes in human brain functional anatomy during nonmotor learning. Cereb Cortex 1994;4(1):8-26. 6. Reivich M, et al. The [18F]fluorodeoxyglucose method for the measurement of local cerebral glucose utilization in man. Circ Res 1979;44(1):127-37. 7. Snow BJ, et al. Human positron emission tomographic [18F]fluorodopa studies correlate with dopamine cell counts and levels. Ann Neurol 1993;34(3):324-30. 8. Firnau G, et al. Cerebral metabolism of 6-[18F]fluoro-L-3, 4-dihydroxyphenylalanine in the primate. J Neurochem 1987;48(4):1077-82. 9. Martin WR, et al. Nigrostriatal function in humans studied with positron emission tomography. Ann Neurol 1989;26(4):535-42. 10. Farde L, et al. Stereoselective binding of 11C-raclopride in living human brain – a search for extrastriatal central D2-dopamine receptors by PET. Psychopharmacology (Berl) 1988;94(4):471-8. 11. Rinne JO, et al. Increased density of dopamine D2 receptors in the putamen, but not in the caudate nucleus in early Parkinson’s disease: a PET study with [11C]raclopride. J Neurol Sci 1995;132(2):156-61. 12. Mukherjee J, et al. Brain imaging of 18F-fallypride in normal volunteers: blood analysis, distribution, testretest studies, and preliminary assessment of sensitivity to aging effects on dopamine D-2/D-3 receptors. Synapse 2002;46(3):170-88.

319

320

22

Diagnostic PET in image guided neurosurgery

13. Ding YS, et al. Pharmacokinetics and in vivo specificity of [11C]dl-threo-methylphenidate for the presynaptic dopaminergic neuron. Synapse 1994;18(2):152-60. 14. Volkow ND, et al. A new PET ligand for the dopamine transporter: studies in the human brain. J Nucl Med 1995;36(12):2162-8. 15. Ciliax BJ, et al. The dopamine transporter: immunochemical characterization and localization in brain. J Neurosci 1995;15(3 Pt 1):1714-23. 16. Lee CS, et al. In vivo positron emission tomographic evidence for compensatory changes in presynaptic dopaminergic nerve terminals in Parkinson’s disease. Ann Neurol 2000;47(4):493-503. 17. Logan J, et al. Graphical analysis of reversible radioligand binding from time-activity measurements applied to [N-11C-methyl]-(-)-cocaine PET studies in human subjects. J Cereb Blood Flow Metab 1990;10(5):740-7. 18. Telang FW, et al. Distribution of tracer levels of cocaine in the human brain as assessed with averaged [11C]cocaine images. Synapse 1999;31(4):290-6. 19. Haaparanta, M., et al. [18F]CFT ([18F]WIN 35,428), a radioligand to study the dopamine transporter with PET: biodistribution in rats. Synapse 1996;23(4):321-7. 20. Koeppe RA, et al. Kinetic evaluation of [11C]dihydrotetrabenazine by dynamic PET: measurement of vesicular monoamine transporter. J Cereb Blood Flow Metab 1996;16(6):1288-99. 21. Chan GL, et al. Reproducibility studies with 11C-DTBZ, a monoamine vesicular transporter inhibitor in healthy human subjects. J Nucl Med 1999;40(2):283-9. 22. Mansour A, et al. Biochemical anatomy: Insights into the cell biology and pharmacology of dopamine and serotonin systems in the brain. In Schatzberg AF, Nemeroff CB, editors. Textbook of psychopharmacology. Washington, DC: American Psychiatric Press; 1998. p. 55-73. 23. Gunn RN, et al. Tracer kinetic modeling of the 5-HT1A receptor ligand [carbonyl-11C]WAY-100635 for PET. Neuroimage 1998;8(4):426-40. 24. Costes, N., et al. A 18F-MPPF PET normative database of 5-HT1A receptor binding in men and women over aging. J Nucl Med 2005;46(12):1980-9. 25. Costes, N., et al. Modeling [18F]MPPF positron emission tomography kinetics for the determination of 5-hydroxytryptamine(1A) receptor concentration with multiinjection. J Cereb Blood Flow Metab 2002;22 (6):753-65. 26. Blin, J., et al. [18F]setoperone: a new high-affinity ligand for positron emission tomography study of the serotonin-2 receptors in baboon brain in vivo. Eur J Pharmacol 1988;147(1):73-82. 27. Kapur, S., et al. Reliability of a simple non-invasive method for the evaluation of 5-HT2 receptors using [18F]-setoperone PET imaging. Nucl Med Commun 1997;18(5):395-9.

28. Hinz, R., et al. Validation of a tracer kinetic model for the quantification of 5-HT(2A) receptors in human brain with [11C]MDL 100,907. J Cereb Blood Flow Metab 2007;27(1):161-72. 29. Rosa-Neto, P., et al. Stability of a-[11C]methyl-L-tryptophan brain trapping in healthy male volunteers. Eur J Nucl Med Mol Imaging 2005;32(10):199-204. 30. Irie, T., et al. , Brain acetylcholinesterase activity: validation of a PET tracer in a rat model of Alzheimer’s disease. J Nucl Med 1996;37(4):649-55. 31. Kilbourn MR, et al. In vivo studies of acetylcholinesterase activity using a labeled substrate, N-[11C]methylpiperdin-4-yl propionate ([11C]PMP). Synapse 1996;22 (2):123-31. 32. Namba H, et al. In vivo measurement of acetylcholinesterase activity in the brain with a radioactive acetylcholine analog. Brain Res 1994;667(2):278-82. 33. Snyder SE, et al. Synthesis of 1-[11C]methylpiperidin-4-yl propionate ([11C]PMP) for in vivo measurements of acetylcholinesterase activity. Nucl Med Biol 1998;25 (8):751-4. 34. Savic I, et al. In-vivo demonstration of reduced benzodiazepine receptor binding in human epileptic foci. Lancet 1988;2(8616):863-6. 35. Richardson MP, et al. Benzodiazepine receptors in focal epilepsy with cortical dysgenesis: an 11C-flumazenil PET study. Ann Neurol 1996;40(2):188-98. 36. Juhasz C, et al. Neuroradiological assessment of brain structure and function and its implication in the pathogenesis of West syndrome. Brain Dev 2001;23(7):488-95. 37. Bressan RA, Pilowsky, LS. Imaging the glutamatergic system in vivo – relevance to schizophrenia. Eur J Nucl Med 2000;27(11):1723-31. 38. Burgess RC. Functional localization by neurophysiologic and neuroimaging techniques. J Clin Neurophysiol 1995;12(5):405. 39. George JS, et al. Mapping function in the human brain with magnetoencephalography, anatomical magnetic resonance imaging, and functional magnetic resonance imaging. J Clin Neurophysiol 1995;12(5):406-31. 40. Simpson GV, et al. Dynamic neuroimaging of brain function. J Clin Neurophysiol 1995;12(5):432-49. 41. Puce A. Comparative assessment of sensorimotor function using functional magnetic resonance imaging and electrophysiological methods. J Clin Neurophysiol 1995;12(5):450-9. 42. Puce A, et al. Functional magnetic resonance imaging of sensory and motor cortex: comparison with electrophysiological localization. J Neurosurg 1995;83(2):262-70. 43. Fried I, et al. Functional MR and PET imaging of rolandic and visual cortices for neurosurgical planning. J Neurosurg 1995;83(5):854-61. 44. Detre JA, et al. Localization of subclinical ictal activity by functional magnetic resonance imaging: correlation with invasive monitoring. Ann Neurol 1995;38(4):618-24.

Diagnostic PET in image guided neurosurgery

45. Ives J.R, et al. Monitoring the patient’s EEG during echo planar MRI. Electroencephalogr Clin Neurophysiol 1993;87(6):417-20. 46. Atlas S.W, et al. Functional magnetic resonance imaging of regional brain activity in patients with intracerebral gliomas: findings and implications for clinical management. Neurosurgery 1996;38(2):329-38. 47. Archip N, et al. Non-rigid alignment of pre-operative MRI, fMRI, and DT-MRI with intra-operative MRI for enhanced visualization and navigation in image-guided neurosurgery. Neuroimage 2007;35(2):609-24. 48. Jones T. The role of positron emission tomography within the spectrum of medical imaging. Eur J Nucl Med 1996;23(2):207-11. 49. Jones T. The imaging science of positron emission tomography. Eur J Nucl Med 1996;23(7):807-13. 50. Jahanshahi M, et al. Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movementrelated potentials in normal and Parkinson’s disease subjects. Brain 1995;118 (Pt 4):913-33. 51. Jenkins IH, et al. Impaired activation of the supplementary motor area in Parkinson’s disease is reversed when akinesia is treated with apomorphine. Ann Neurol 1992;32(6):749-57. 52. Dagher A, Nagano-Saito A. Functional and anatomical magnetic resonance imaging in Parkinson’s disease. Mol Imaging Biol 2007;9(4):234-42. 53. Grafton ST. Contributions of functional imaging to understanding parkinsonian symptoms. Curr Opin Neurobiol 2004;14(6):715-9. 54. Ceballos-Baumann AO. Functional imaging in Parkinson’s disease: activation studies with PET, fMRI and SPECT. J Neurol 2003;250 Suppl 1:I15-I23. 55. van Eimeren T, Siebner HR. An update on functional neuroimaging of parkinsonism and dystonia. Curr Opin Neurol 2006;19(4):412-9. 56. Hughes AJ, et al. Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 1992;55 (3):181-4. 57. Heiss WD, Hilker R. The sensitivity of 18-fluorodopa positron emission tomography and magnetic resonance imaging in Parkinson’s disease. Eur J Neurol 2004;11(1):5-12. 58. Leenders KL, et al. Brain dopamine metabolism in patients with Parkinson’s disease measured with positron emission tomography. J Neurol Neurosurg Psychiatry 1986;49(8):853-60. 59. Nahmias C, et al. Striatal dopamine distribution in parkinsonian patients during life. J Neurol Sci 1985;69(3):223-30. 60. Damier P, et al. The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson’s disease. Brain 1999;122 (Pt 8):1437-48.

22

61. Garnett ES, et al. A rostrocaudal gradient for aromatic acid decarboxylase in the human striatum. Can J Neurol Sci 1987;14 Suppl 3:444-7. 62. Daniel SE. de Bruin VM, Lees AJ. The clinical and pathological spectrum of Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy): a reappraisal. Brain 1995;118(Pt 3):759-70. 63. Ghaemi, M, et al. Differentiating multiple system atrophy from Parkinson’s disease: contribution of striatal and midbrain MRI volumetry and multi-tracer PET imaging. J Neurol Neurosurg Psychiatry 2002;73 (5):517-23. 64. Frost JJ, et al. Positron emission tomographic imaging of the dopamine transporter with 11C-WIN 35,428 reveals marked declines in mild Parkinson’s disease. Ann Neurol 1993;34(3):423-31. 65. Brooks DJ. Diagnosis and management of atypical parkinsonian syndromes. J Neurol Neurosurg Psychiatry 2002;72(90001):10i-16i. 66. Antonini A, et al. Complementary PET studies of striatal neuronal function in the differential diagnosis between multiple system atrophy and Parkinson’s disease. Brain 1997;120(Pt 12):2187-95. 67. Otsuka M, et al. Differentiating between multiple system atrophy and Parkinson’s disease by positron emission tomography with 18F-dopa and 18F-FDG. Ann Nucl Med 1997;11(3):251-7. 68. Antonini A, et al. Differential diagnosis of parkinsonism with [18F]fluorodeoxyglucose and PET. Mov Disord 1998;13(2):268-74. 69. Laureys S, et al. Fluorodopa uptake and glucose metabolism in early stages of corticobasal degeneration. J Neurol 1999;246(12):1151-8. 70. Booij J, et al. Imaging of the dopaminergic neurotransmission system using single-photon emission tomography and positron emission tomography in patients with parkinsonism. Eur J Nucl Med 1999;26(2):171-82. 71. Piccini P, Whone A. Functional brain imaging in the differential diagnosis of Parkinson’s disease. Lancet Neurol 2004;3(5):284-90. 72. Herholz K. PET studies in dementia. Ann Nucl Med 2003;17(2):79-89. 73. Silverman DH. Brain 18F-FDG PET in the diagnosis of neurodegenerative dementias: comparison with perfusion SPECT and with clinical evaluations lacking nuclear imaging. J Nucl Med 2004;45(4):594-607. 74. Devous MD Sr. Functional brain imaging in the dementias: role in early detection, differential diagnosis, and longitudinal studies. Eur J Nucl Med Mol Imaging 2002;29(12):1685-96. 75. Van Heertum RL, Tikofsky RS. Positron emission tomography and single-photon emission computed tomography brain imaging in the evaluation of dementia. Semin Nucl Med 2003;33(1):77-85.

321

322

22

Diagnostic PET in image guided neurosurgery

76. Ishii K, Minoshima S. PET is better than perfusion SPECT for early diagnosis of Alzheimer’s disease. Eur J Nucl Med Mol Imaging 2005;32(12):1463-5. 77. Jagust WJ, et al. The cortical topography of temporal lobe hypometabolism in early Alzheimer’s disease. Brain Res 1993;629(2):189-98. 78. Fukuyama H, et al. Altered cerebral energy metabolism in Alzheimer’s disease: a PET study. J Nucl Med 1994;35(1):1-6. 79. Minoshima S, et al. Metabolic reduction in the posterior cingulate cortex in very early Alzheimer’s disease. Ann Neurol 1997;42(1):85-94. 80. Albin RL, et al. Fluoro-deoxyglucose positron emission tomography in diffuse Lewy body disease. Neurology 1996;47(2):462-6. 81. Imamura T, et al. Regional cerebral glucose metabolism in dementia with Lewy bodies and Alzheimer’s disease: a comparative study using positron emission tomography. Neurosci Lett 1997;235(1–2):49-52. 82. Ishii K, et al. Regional cerebral glucose metabolism in dementia with Lewy bodies and Alzheimer’s disease. Neurology 1998;51(1):125-30. 83. Higuchi M, et al. Glucose hypometabolism and neuropathological correlates in brains of dementia with Lewy bodies. Exp Neurol 2000;162(2):247-56. 84. Friedland RP, et al. Functional imaging, the frontal lobes, and dementia. Dementia 1993;4(3–4):192-203. 85. Herholz K. FDG PET and differential diagnosis of dementia. Alzheimer Dis Assoc Disord 1995;9(1):6-16. 86. McKeith IG, et al. Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 2005;65(12):1863-72. 87. Rowe CC, et al. Imaging b-amyloid burden in aging and dementia. Neurology 2007;68(20):1718-25. 88. Engler H, et al. In vivo amyloid imaging with PET in frontotemporal dementia. Eur J Nucl Med Mol Imaging 2008;35(1):100-6. 89. Di Chiro G, Brooks RA. PET-FDG of untreated and treated cerebral gliomas. J Nucl Med 1988;29(3):421-3. 90. Delbeke D, et al. Optimal cutoff levels of F-18 fluorodeoxyglucose uptake in the differentiation of low-grade from high-grade brain tumors with PET. Radiology 1995;195(1):47-52. 91. Ogawa T, et al. Quantitative evaluation of neutral amino acid transport in cerebral gliomas using positron emission tomography and fluorine-18 fluorophenylalanine. Eur J Nucl Med 1996;23(8):889-95. 92. Kaschten B, et al. Preoperative evaluation of 54 gliomas by PET with fluorine-18-fluorodeoxyglucose and/or carbon-11-methionine. J Nucl Med 1998;39(5):778-85. 93. Chung JK, et al. Usefulness of 11C-methionine PET in the evaluation of brain lesions that are hypo- or isometabolic on 18F-FDG PET. Eur J Nucl Med Mol Imaging 2002;29(2):176-82.

94. Pauleit D, et al. O-(2-[18F]fluoroethyl)-L-tyrosine PET combined with MRI improves the diagnostic assessment of cerebral gliomas. Brain 2005;128(Pt 3):678-87. 95. Derlon JM, et al. [11C]L-methionine uptake in gliomas. Neurosurgery 1989;25(5):720-8. 96. Ogawa T, et al. Cerebral glioma: evaluation with methionine PET. Radiology 1993;186(1):45-53. 97. Nuutinen, J., et al. Radiotherapy treatment planning and long-term follow-up with [11C]methionine PET in patients with low-grade astrocytoma. Int J Radiat Oncol Biol Phys 2000;48(1):43-52. 98. De Witte O, et al. Positron emission tomography with injection of methionine as a prognostic factor in glioma. J Neurosurg 2001;95(5):746-50. 99. Ribom D, et al. Positron emission tomography 11C-methionine and survival in patients with low-grade gliomas. Cancer 2001;92(6):1541-9. 100. Levivier M, et al. Positron emission tomographyguided stereotactic brain biopsy. Neurosurgery 1992; 31(4):792-7; 101. Pirotte B, et al. PET in stereotactic conditions increases the diagnostic yield of brain biopsy. Stereotact Funct Neurosurg 1994;63(1–4):144-9. 102. Pirotte B, et al. Use of positron emission tomography (PET) in stereotactic conditions for brain biopsy. Acta Neurochir (Wien) 1995;134(1–2):79-82. 103. Levivier M, et al. Diagnostic yield of stereotactic brain biopsy guided by positron emission tomography with [18F]fluorodeoxyglucose. J Neurosurg 1995; 82(3):445-52. 104. Goldman S, et al. Regional methionine and glucose uptake in high-grade gliomas: a comparative study on PET-guided stereotactic biopsy. J Nucl Med 1997; 38(9):1459-62. 105. Pirotte B, et al. Combined positron emission tomography and magnetic resonance imaging for the planning of stereotactic brain biopsies in children: experience in 9 cases. Pediatr Neurosurg 2003;38(3):146-55. 106. Spence AM, Mankoff DA, Muzi M. Positron emission tomography imaging of brain tumors. Neuroimaging Clin N Am 2003;13(4):717-39. 107. Schaller B. Usefulness of positron emission tomography in diagnosis and treatment follow-up of brain tumors. Neurobiol Dis 2004;15(3):437-48. 108. Holzer T, et al. FDG-PET as a prognostic indicator in radiochemotherapy of glioblastoma. J Comput Assist Tomogr 1993;17(5):681-7. 109. Francavilla TL, et al. Positron emission tomography in the detection of malignant degeneration of low-grade gliomas. Neurosurgery 1989;24(1):1-5. 110. Ricci PE, et al. Differentiating recurrent tumor from radiation necrosis: time for re-evaluation of positron emission tomography? AJNR Am J Neuroradiol 1998;19(3):407-13.

Diagnostic PET in image guided neurosurgery

111. Tsuyuguchi N, et al. Methionine positron emission tomography for differentiation of recurrent brain tumor and radiation necrosis after stereotactic radiosurgery in malignant glioma. Ann Nucl Med 2004; 18(4):291-6. 112. Carne RP, et al. MRI-negative PET-positive temporal lobe epilepsy: a distinct surgically remediable syndrome. Brain 2004;127(10):2276-2285. 113. Casse R, et al. Positron emission tomography and epilepsy. Mol Imaging Biol 2002;4(5):338-51. 114. Juhasz C, et al. Glucose and [11C]flumazenil positron emission tomography abnormalities of thalamic nuclei in temporal lobe epilepsy. Neurology 1999; 53(9):2037-45. 115. Koepp M.J, et al. 11C-flumazenil PET in patients with refractory temporal lobe epilepsy and normal MRI. Neurology 2000;54(2):332-9. 116. O’Brien TJ, et al. The utility of a 3-dimensional, largefield-of-view, sodium iodide crystal-based PET scanner in the presurgical evaluation of partial epilepsy. J Nucl Med 2001;42(8):1158-65. 117. Kuhl DE, et al. Epileptic patterns of local cerebral metabolism and perfusion in humans determined by emission computed tomography of 18FDG and 13NH3. Ann Neurol 1980;8(4):348-60. 118. Ollenberger GP, et al. Assessment of the role of FDG PET in the diagnosis and management of children with refractory epilepsy. Eur J Nucl Med Mol Imaging 2005;32(11):1311-6. 119. Koepp MJ, Woermann FG. Imaging structure and function in refractory focal epilepsy. Lancet Neurol 2005;4(1):42-53. 120. Savic I, Ingvar M, Stone-Elander S. Comparison of [11C]flumazenil and [18F]FDG as PET markers of epileptic foci. J Neurol Neurosurg Psychiatry 1993;56 (6):615-21. 121. Arnold S, et al. Reduction of benzodiazepine receptor binding is related to the seizure onset zone in extratemporal focal cortical dysplasia. Epilepsia 2000; 41(7):818-24. 122. Muzik O, et al. Intracranial EEG versus flumazenil and glucose PET in children with extratemporal lobe epilepsy. Neurology 2000;54(1):171-9. 123. Yousry TA, et al. Topography of the cortical motor hand area: prospective study with functional MR imaging and direct motor mapping at surgery. Radiology 1995; 195(1):23-9. 124. Majos, A, et al. Cortical mapping by functional magnetic resonance imaging in patients with brain tumors. Eur Radiol 2005;15(6):1148-58. 125. Roessler, K, et al. Evaluation of preoperative high magnetic field motor functional MRI (3 Tesla) in glioma patients by navigated electrocortical stimulation and postoperative outcome. J Neurol Neurosurg Psychiatry 2005;76(8):1152-7.

22

126. Kloppel S, Buchel C. Alternatives to the Wada test: a critical view of functional magnetic resonance imaging in preoperative use. Curr Opin Neurol 2005;18(4):418-23. 127. Kaplan AM, et al. Functional brain mapping using positron emission tomography scanning in preoperative neurosurgical planning for pediatric brain tumors. J Neurosurg 1999;91(5):797-803. 128. Meyer PT, et al. Preoperative mapping of cortical language areas in adult brain tumour patients using PET and individual non-normalised SPM analyses. Eur J Nucl Med Mol Imaging 2003;30(7):951-60. 129. Vanlancker-Sidtis D. McIntosh AR, Grafton S. PET activation studies comparing two speech tasks widely used in surgical mapping. Brain Lang 2003;85 (2):245-61. 130. Limousin P, et al. Changes in cerebral activity pattern due to subthalamic nucleus or internal pallidum stimulation in Parkinson’s disease. Ann Neurol 1997;42 (3):283-91. 131. Ceballos-Baumann AO, et al. A positron emission tomographic study of subthalamic nucleus stimulation in Parkinson disease: enhanced movement-related activity of motor-association cortex and decreased motor cortex resting activity. Arch Neurol 1999;56(8):997-1003. 132. Strafella AP, Dagher A, Sadikot AF. Cerebral blood flow changes induced by subthalamic stimulation in Parkinson’s disease. Neurology 2003;60(6):1039-42. 133. Davis KD, et al. Activation of the anterior cingulate cortex by thalamic stimulation in patients with chronic pain: a positron emission tomography study. J Neurosurg 2000;92(1):64-9. 134. Strafella AP, et al. Subdural motor cortex stimulation in Parkinson’s disease does not modify movement-related rCBF pattern. Mov Disord 2007;22(14):2113-6. 135. Roberto Cilia ALFVESGPAA. Extradural motor cortex stimulation in Parkinson’s disease. Mov Disord 2007; 22(1):111-114. 136. Mayberg HS, et al. Deep brain stimulation for treatment-resistant depression. Neuron 2005;45(5):651-60. 137. May A, et al. Hypothalamic activation in cluster headache attacks. Lancet 1998;352(9124):275-8. 138. Leone M, Franzini A, Bussone G. Stereotactic stimulation of posterior hypothalamic gray matter in a patient with intractable cluster headache. N Engl J Med 2001;345(19):1428-9. 139. Leone M, et al. Hypothalamic deep brain stimulation for intractable chronic cluster headache: a 3-year follow-up. Neurol Sci 2003;24 Suppl 2:S143-S145. 140. Franzini A, et al. Stimulation of the posterior hypothalamus for treatment of chronic intractable cluster headaches: first reported series. Neurosurgery 2003;52 (5):1095-9; 141. Herholz K, Coope D, Jackson A. Metabolic and molecular imaging in neuro-oncology. Lancet Neurol 2007; 6(8):711-24.

323

20 Functional MRI in Image Guided Neurosurgery T. Sankar . G. R. Cosgrove

Introduction The principal goal of neurosurgical procedures on the cerebral cortex is to accurately localize and maximally resect lesions or abnormal tissue. An intimate knowledge of eloquent cortical regions which may be damaged during surgery is therefore a prerequisite for safe cortical neurosurgery. Identifying functionally important areas of the cortex during surgery can be aided by a priori knowledge of cortical functional organization, but is subject to inaccuracy caused by individual variations in anatomy and displacement of normal structures by pathological lesions. Consequently, several cortical mapping techniques have been established to facilitate safe and effective cortical resections. The gold standard for cortical mapping is direct electrocortical stimulation (ECS) of the exposed cortex at surgery [1–3]. ECS is limited, however, because it is an invasive technique which can usually only be performed in an awake patient [3]. Awake craniotomy is not always feasible and presents unique anesthetic and analgesic challenges. In addition, as a surface mapping technique, ECS cannot provide information about function buried within the sulcal depths which represent a substantial proportion of the cortical volume [4]. Perhaps most importantly, ECS is a purely intra-operative technique which cannot be used preoperatively to guide surgical planning [3]. The past two decades have seen the development and implementation of several noninvasive cortical mapping techniques, including positron emission tomography (PET), #

Springer-Verlag Berlin/Heidelberg 2009

magnetoencephalography (MEG), and transcranial magnetic stimulation (TMS) [3]. Functional magnetic resonance imaging (fMRI), which assesses regional variations in cerebral blood flow during various tasks of cortical activation, is one such technique. fMRI makes use of readily available conventional MRI hardware to produce maps of functional cortical activation, which can be superimposed onto anatomical images of the brain. The resulting structural and functional model of the brain – which is obtained prior to surgery – can then be used both for preoperative surgical planning and intra-operative decisionmaking. Recent clinical experience in patients with lesions involving eloquent cortex has demonstrated the utility of fMRI in the neurosurgical armamentarium.

Principles of fMRI Acquisition Physiological Basis of fMRI Basic neurophysiologic studies have long shown that cerebral activity is tightly coupled to cerebral metabolism, which is in turn related to cerebral blood flow [5]. As a result, regionalhemodynamic measurements can serve as a surrogate marker of neuronal activity. This principle forms the basis of metabolic/hemodynamic mapping techniques such as PET [6] and fMRI [7]. In 1991, Belliveau et al. [8] first reported on the use of this principle in MR imaging. After intravenous bolus injection of a paramagnetic contrast agent, they rapidly acquired MR images and demonstrated signal change in the visual

288

20

Functional MRI in image guided neurosurgery

cortex due to activation with photic stimulation. This signal change was presumed to be due to increased concentration of contrast agent accompanying increased regional blood flow to the visual cortex, and became known as the ‘‘contrast bolus tracking’’ technique. fMRI based on contrast bolus tracking is seldom used today. The most commonly used fMRI acquisition method measures blood oxygen level-dependent (BOLD) changes in the magnetic resonance (MR) signal, first described by Ogawa et al. [9,10]. BOLD imaging has become the fMRI acquisition technique of choice because it does not require the administration of an exogenous contrast agent. An increase in neuronal activity in a particular region of the brain – caused by, say, performing a particular task – initially leads to a transient increase in oxygen extraction from the blood supply to that region. This is quickly followed by compensatory vasodilation, which produces a net increase in the overall concentration of oxy-hemoglobin (oxy-Hb) relative to deoxy-hemoglobin (deoxy-Hb) [7,11]. The physiologic mechanisms underpinning this vasodilatory response are not yet fully understood, but various locally-generated chemical mediators have been implicated, including serotonin, acetylcholine, neuroactive peptides, and nitric oxide produced by cortical neurons [12]. Since the iron in deoxy-Hb is paramagnetic, it reduces T2 MR signal through spin-dephasing effects. The relative decrease in deoxy-Hb concentration in a region of increased neuronal activity, then, produces a corresponding increase in T2 signal, forming the basis of BOLD imaging [9]. This T2 signal change is primarily thought to come from the microvasculature consisting of the capillary system and small venules, and is of low magnitude (on the order of 0.5–5%) [13]. Studies in both humans and primates have demonstrated that the BOLD signal is proportional to the neuronal firing rate, though the latency of the observed change is on the order of several seconds [14,15].

Technological Requirements for fMRI Acquisition Given the small magnitude of changes in the BOLD signal accompanying neuronal activation, signal-to-noise ratio is of critical importance during fMRI acquisition. Initial fMRI studies were carried out using high field strength magnets (2–4 T) using standard gradient-echo acquisitions. Subsequent improvements in gradient coil shielding and surface coil design allowed conventional 1.5 T scanners to be used, but at the expense of prolonged and frequently impractical acquisition times [16]. The recent development and application of echo-planar imaging gradients has revolutionized fMRI acquisition, allowing entire volumes to be imaged in seconds, with improved spatial resolution and signal-tonoise [17]. Most current fMRI studies are carried out on conventional 1.5 T MRI scanners with modifications to allow for echo-planar imaging, and involve multiple iterations of image acquisition and task repetition [7]. Following acquisition, fMRI data must be processed and displayed in a format suitable for clinical use. Typically, a conventional desktop computer workstation equipped with imageprocessing software is used to average multiple fMRI acquisitions. Next, voxel-by-voxel analysis is performed to identify those cortical regions which have an increased BOLD signal relative to baseline during performed tasks. The threshold used to classify increased signal as true cortical activation is arbitrary; normally, statistical methods are used to select a threshold coefficient 2–3 standard deviations from baseline. fMRI images are then co-registered, fused, and volume rendered with anatomical MRI images using both surface- and volume-based matching techniques [18]. Images of regions of cortical activation can then be superimposed onto anatomical images for display purposes or incorporated into neuronavigation systems for intra operative surgical guidance [19] (> Figure 20‐1).

Functional MRI in image guided neurosurgery

20

. Figure 20‐1 fMRI of sensorimotor hand and foot activation superimposed on axial T2 weighted images demonstrating a tumor in the left posterior superior frontal gyrus just anterior to the motor strip. Note that the right foot activation is less intense and pushed posteriorly by the tumor

Task Design and Selection For neurosurgical mapping purposes, fMRI data are generated using a block design paradigm. Simply, block design involves multiple trials of a task or stimulus presentation – a so-called ‘‘task block’’ – alternating with multiple trials of a control task (‘‘control block’’) [3,20,21]. The resulting BOLD signals from task and control blocks are compared, allowing for the detection of subtle changes accompanying task-related cerebral activation. There is no standardization of the length of each task block or the number of alternating cycles between task and control blocks. Typically, task blocks last from 15 to 30 s; this ensures that they are of sufficient duration to allow the occurrence of hemodynamic changes underlying the fMRI signal [7,22,23]. Cycling multiple trials of a task block with control blocks improves signal-tonoise ratio and the overall statistical accuracy of inferred cortical activations [24] (> Figure 20‐2). Several task variants have been developed to assess cortical activation in different functional regions of the brain, including the sensorimotor cortex, the speech areas of Broca and Wernicke, and the primary visual cortex. The classical motor

activation task is finger-thumb tapping, though repetitive clenching of the fingers or sponge squeezing have also been employed. It is important to realize that this motor task includes stimulation of both cutaneous and proprioceptive sensory inputs and therefore is more accurately a combined sensorimotor task than a pure motor task. Sensory stimulation is frequently achieved by brushing of the palmar surface of the hand [7]. Language is assessed by picture naming, verb generation, or having the patient classify related nouns into categories [25–27]. Because of the motion artifact created by speech, most centers favor of using silent instead of vocalized speech for language mapping [27]. Visual tasks frequently involve intermittent photic stimulation with patterned stimuli presented via binoculars or on a screen [22].

Application of fMRI to Cortical Resections Illustrative Cases Case # 1 – This 17-year-old male had experienced intractable seizures for nearly 10 years which

289

290

20

Functional MRI in image guided neurosurgery

. Figure 20‐2 Demonstration of the signal changes on fMRI during activation task versus resting state cycle

were characterized by the sudden onset of dystonic posturing and elevation of his right upper extremity followed by rapid secondary generalization. Video EEG recordings suggested a left frontal or bifrontal onset and MRI demonstrated a non-enhancing lesion in the left frontal parasaggital cortex. Functional MRI was carried out for sensorimotor testing of the right hand and the results mapped to the patients structural MRI. At surgery, direct ECS of the exposed cortex confirmed the location of primary sensorimotor cortex of the hand region in the pre and post central gyri. A 4 contact depth electrode was then placed in the region of the presumed supplementary motor area (SMA) and stimulation through the deepest and middle contacts elicited tonic contraction and elevation of the entire right upper extremity consistent with a SMA type seizure (> Figure 20‐3). Careful resection of the cortex just anterior to the SMA revealed a ganglioglioma and the patient has remained seizure free for nearly a decade. Case # 2 – This 24-year-old right-handed man had noticed episodes of sudden onset of a ‘‘tickling’’ in his throat followed by reflexive coughing and some slight difficulty speaking within the past year. These episodes would last for just a few minutes and occur irregularly. After

one such episode, he experienced a generalized tonic conic convulsion and he was taken to a local emergency room where an enhancing lesion was discovered in his dominant subcentral gyrus. A functional MRI was performed for sensorimotor tongue activation and for language mapping using a visual verb generation task (> Figure 20‐4a). At surgery under local anesthesia, cortical mapping of tongue sensorimotor and language areas corresponded closely to that predicted by fMRI. The location of the tumor could be easily determined by the gyral anatomy and cortical vessels and was resected without deficit (> Figure 20‐4b). Pathology demonstrated an xanthoastrocytoma and the patient has been seizure free since surgery. Case #3 – This 47-year-old bilingual, righthanded Greek woman had previously undergone resection of an oligodendroglioma 5 years before presenting with a recurrent tumor. Functional MRI was performed using visual and auditory verb generation tasks in both English and Greek (> Figure 20‐5a). These results were mapped to a structural MRI of her brain and at surgery under local anesthesia correlated closely with language mapping in both languages with ECS enabling safe resection of the recurrent tumor (> Figure 20‐5b).

Functional MRI in image guided neurosurgery

20

. Figure 20‐3 (a) Axial and (b) surface rendered MRI images with superimposed fMRI activations demonstrating a tumor in the superior left frontal gyrus and both primary and supplementary motor area activations during hand movement (c) cropped close up view of cortical surface as predicted by fMRI as compared to (d) intraoperative view of cortical surface with green tags indicating motor responses in the hand, white tags motor responses in the proximal upper extremity and red tag the area where depth electrode stimulation elicited SMA type seizure. Asterisks are for localization purposes but gyral anatomy and cortical veins are also useful

Discussion Sensitivity and Interpretation of fMRI Results According to Kim and Singh [7], the tasks used for fMRI data generation can be considered either simple or complex, based on the area of cortex they consistently activate. For example, finger-thumb tapping is considered a simple motor task, which typically activates a welldefined focal area of motor cortex. However, even so called simple motor tasks are actually a combination of both motor and sensory activations because of the activation of cutaneous and proprioceptive input. Complex tasks such as

language function require simultaneous activation of several regions of the brain, each with multiple sensory inputs and functional outputs. However, even simple tasks may require supplementary areas whose interaction with the primary cortical activation area is poorly understood. Furthermore, in order to increase the overall sensitivity of fMRI, some centers assess cortical activation during tasks completed in both active and passive modes (e.g., spoken and silent speech), because redundancy is thought to exist in functional areas of cortical activation for related tasks [7]. As a consequence of these factors, preoperative fMRI imaging maps frequently demonstrate a greater spread and area of activation than do

291

292

20

Functional MRI in image guided neurosurgery

. Figure 20‐4 (a) Axial MRI images of enhancing nodule in left central region and the surface rendered fMRI of the whole brain with tumor in yellow, tongue activation in pink and verb generation task activation in green (b) images of the cortical surface at surgery and that predicted by fMRI cropped for comparison. Note the excellent correlation between ECS and fMRI. The subcortical location of the tumor is easily deduced from the surface anatomy

invasive intraoperative mapping techniques such as ECS, and it is occasionally unclear which cortical regions are essential to the completion of a given task. Optimum interpretation of preoperative fMRI is predicated, then, on a reasoned consideration of the balance between increased sensitivity generated by task complexity or redundancy on the one hand, and a priori knowledge of functional neuroanatomy on the other. Keeping these principles in mind, the overall sensitivity of fMRI is usually reported as excellent. In a widely cited report, Hirsch et al. [28] were able to demonstrate 100% sensitivity for identifying language cortex in the superior temporal gyrus, motor

function in the precentral gyrus, and visual function in occipital cortex. They also showed 93% sensitivity for Broca’s area.

Comparison of Functional Cortical Localization Between fMRI and ECS Several studies have attempted to validate fMRI data by comparing it against standard cortical localization by ECS. The definition of adequate correlation between the two techniques varies from study to study, but most authors consider

Functional MRI in image guided neurosurgery

20

. Figure 20‐5 (a) fMRI images of cortical activation during language tasks in both English and Greek. Note that the auditory verb generation task activates primary auditory cortex in addition to anterior language areas (b) images of the cortical surface cropped for comparison to that predicted by fMRI. Both the structural and functional correlation is excellent

correlation to be successful when both techniques demonstrate functional localization to within some arbitrary distance of one another, usually 10 or 20 mm. Most existing studies have focused on sensorimotor mapping, and have almost uniformly reported excellent correlation between the two techniques [28–39]. In particular, fMRI appears to be particularly successful at correctly identifying the central sulcus (CS): Majos et al. [35] reported a 98% success rate in mapping

the CS, and Lehericy et al. [32] showed a similar concordance rate of 92% in a large study of 60 patients. Furthermore, brain distortion as a result of edema and deformation due to tumors or other pathological entities does not seem to impact this concordance. Hirsch et al. [28] reported that overall localization of the CS was possible in 97% of patients being surgically treated for lesions of the central region. Excellent sensorimotor functional correlation has also been observed in the hand

293

294

20

Functional MRI in image guided neurosurgery

area located within the pli de passage moyen (PPM) of the precentral gyrus [37], even in the presence of infiltrative glioma [36]. Interestingly, Boling et al. [40] recently used fMRI to demonstrate that there may be a distinct whole hand sensory and motor area within the PPM. To date, agreement between fMRI and ECS has been less robust for language localization. Some studies have indeed reported excellent concordance with word-generation tasks for mapping Broca’s area [28,29,41], as well as for language function in general using a battery of tasks [42]. The most recent and systematic study directly comparing language localization by both methods was published by Roux et al. [43], who examined a series of 14 right-handed patients – all with tumors in the left hemisphere – with preoperative fMRI obtained during naming and verb generation tasks. During operative tumor resection, they also assessed 426 distinct cortical sites by ECS across the patient cohort. In total, 22 sites were found to be ‘‘positive’’ during naming or verb generation (i.e., elicited speech arrest, anomia, hesitations, paraphasic errors, or delayed responses when stimulated). Of these, only 13 (59%) were concordant (i.e., within 1 cm of) with fMRI signals. The authors concluded from these data that fMRI itself is insufficient to make critical surgical decisions in essential cortical language areas. However, the study suffered from some methodological limitations which weakened its dismissal of fMRI for language mapping. Specifically, the study did not use a silent speech generation task during fMRI acquisition, thereby ignoring the principle of task redundancy and increasing susceptibility to motion artifact. In addition, as noted by McKhann II and Hirsch [44] in their comment on the study, language disruption sites within dominant face motor cortex were included among the 22 positive stimulation sites. Normally, fMRI obtained with silent speech tasks does not activate motor cortex, suggesting that the methods may have been inherently biased against the accuracy of fMRI for language. That being

said, recent work has suggested that the weakness of silent speech tasks may lie in their inability to activate contributory cortical sites within the precentral gyrus [45]. Clearly, further work needs to be done to elucidate the optimal testing paradigms which generate the most accurate preoperative fMRI maps of cortical language localization across a varied population of patients. Such work may solidify the value of fMRI in guiding cortical resections in language-specific regions. Currently, all fMRI results for language should be interpreted with caution and must still be validated intra-operatively with ECS in the awake patient.

Advantages of fMRI as a Cortical Mapping Technique in Neurosurgery fMRI has as its principal advantage the fact that it is non-invasive, which significantly increases its safety and repeatability compared to direct ECS. At best, intraoperative testing requires a larger craniotomy, increases operative time, and is associated with significant patient stress and discomfort accompanying an awake procedure under local anesthetic. At worst, ECS may be associated with intraoperative seizures which may force premature termination of mapping or require the procedure to be aborted altogether [3,46]. Furthermore, awake craniotomy generally requires dedicated neuroanesthesia support and sufficient experience which may preclude its use in smaller centers. fMRI has good spatial resolution, estimated to be on the order of 2–5 mm [47]; this is well within the 10 mm spread of electrical current to adjacent cortical areas when ECS is used [7]. fMRI also has the advantage of generating data over the entire extent of the brain, producing global maps of cortical activation. This data can be important even if we concede that the accuracy of fMRI for precise functional localization may

Functional MRI in image guided neurosurgery

be uncertain [22]. Invasive mapping is typically performed if a proposed resection is believed, preoperatively, to place eloquent cortex at risk. fMRI can hence be used prior to surgery to identify patients in whom invasive intraoperative mapping will be required, avoiding in others the significant risks and increased operative time required by such mapping [48]. This complementary application of fMRI confirms its worth even as work continues to establish it as a cortical mapping technique independent of other imaging or stimulatory modalities. Perhaps the most appealing feature of fMRI is that it can demonstrate cortical activation within the sulcal depths, which have been reported to represent as much as two-thirds of functionally eloquent cortex [4]. This is a clear advantage over ECS, which can only assess surface cortex. The ability of fMRI to guide preservation of cortical grey matter in the deep sulci during surgery may be of particular relevance to avoiding damage to cognitive and memory functions, whose underlying neuroanatomical basis is poorly understood [3,7].

Disadvantages of fMRI in Neurosurgical Applications While fMRI can localize distinct cortical activity, it does not localize underlying white matter tracts or the important connections between functional areas. The risks of incurring neurological deficits are often greatest during subcortical resections in the white matter and therefore careful consideration of the location of these pathways must always be paramount. Only surgery performed under local anesthesia with constant testing of the patient’s function during resection can prevent deficits and therefore fMRI will never completely replace standard ECS. Most shortcomings of fMRI are technical. As with any preoperative imaging modality, fMRI is susceptible to inaccuracies because of the brain

20

shift accompanying craniotomy, dural opening, and CSF drainage [49]. Sensitivity to motion artifact, which is principally caused by a patient’s inability to hold the head still, or occasionally by involuntary movements related to breathing or heartbeat, can also be problematic [3,22]. As mentioned previously, during tasks involving overt speech, word vocalization may alone produce sufficient motion to degrade image acquisition and quality. The rapid image acquisition achieved with echoplanar technology partially reduces the impact of motion on fMRI studies. Firmly securing the head and providing a visual fixation crosshair may also help [28,42], but occasionally – particularly in cognitively impaired or uncooperative patients – an fMRI examination simply cannot be completed. Venous effects may also confuse fMRI interpretation. While fMRI is based on the assumption that the BOLD signal is confined to the microvasculature, in reality there is signal spread to veins draining blood away from activated cortical tissue and which may be located several millimeters from the actual focus of neuronal activation. This signal in turn can produce images depicting false-positive activation in these adjacent regions [50]. Obtaining highquality three dimensional anatomic MRI images showing the positions of draining veins can assist the neurosurgeon in anticipating areas of falsepositive signal [4]. In addition, venous signal appears to be less of an issue at higher magnetic field strength [50]. Related to aberrant venous signal is the theoretical possibility that various neurosurgical pathologies may alter normal blood flow in such a way as to disrupt fMRI interpretation. One such example of this phenomenon is the effect of tumor angiogenesis, whose impact on the BOLD signal is as yet unknown. Vascular steal related to arteriovenous malformations near eloquent cortex has similarly been cited as another potential pitfall [7]. Even atherosclerotic disease may potentially impact regional variations

295

296

20

Functional MRI in image guided neurosurgery

in blood flow from individual to individual, and within the same individual at different times. Further study is necessary to assess the BOLD signal in these clinical situations to appropriately interpret fMRI data prior to surgical resections. As mentioned previously, perhaps the greatest current limitation of fMRI for guiding cortical resections relates to the – as yet – uncertain neuroscientific implications of the data it generates. At present, we cannot use fMRI to accurately distinguish between essential functional cortical areas and those which are participatory but nonessential to function [7]. This is certainly true for language, but even more so for memory, whose neuroanatomic basis is still incompletely understood [51]. Fortunately, fMRI data are being analyzed in the setting of several neuropsychological and cognitive functions, and the conclusions reached from this basic work will likely make their way into neurosurgical applications. Additionally, the ongoing development of increasingly standardized fMRI task protocols should help to improve the interpretation and reproducibility of cortical mapping data between different patients and different centers.

Conclusions fMRI is a powerful non-invasive neuroimaging technique that can create a unique structural and functional model of an individual patient’s brain. The widespread availability of MRI scanners allows fMRI exams to be acquired in appropriate patients at most modern neurosurgical centers. fMRI data are generated preoperatively and can be used to determine the feasibility of open cortical resections by delineating those areas of eloquent cortex which may be at risk in a planned surgical procedure. Such data can be of critical importance in assessing surgical risk, optimizing surgical exposure, as well as guiding surgical approaches to and the resection of cortical

lesions. fMRI has several advantages over ECS, including its non-invasiveness, its higher spatial resolution, and its ability to assess function within the sulcal depths. fMRI acquisitions can be impaired, however, by technical factors such as motion artifact, infiltrative tumors and venous effects, and fMRI data are not perfectly correlated with ECS, particularly for language localization. Future investigations will likely establish the appropriate task paradigms required to maximize the accuracy of functional cortical maps generated by fMRI. Meanwhile, fMRI has already come into widespread use in neurosurgery, either independently or as an adjunct to ECS. The future of cortical neurosurgery is one in which all patients will routinely undergo fMRI as part of their presurgical evaluation.

References 1. Penfield W. The cerebral cortex and consciousness, in the Harvey lectures. Baltimore: Williams & Wilkins Co.; 1937. p. 35-69. 2. Ojemann G, Ojemann J, Lettich E, Berger M. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 1989;71:31-326. 3. Tharin S, Golby A. Functional brain mapping and its applications to neurosurgery. Neurosurgery 2007;60(4 Suppl 2):185-201. 4. Cosgrove GR, Buchbinder BR, Jiang H. Functional magnetic resonance imaging for intracranial navigation. Neurosurg Clin N Am 1996;7:313-22. 5. Colebatch JG, Deiber M-P, Passingham RE, Friston KJ, Frackowiak KS. Regional cerebral blood flow during voluntary arm and hand movements in human subjects. J Neurophysiol 1991;65:1392-401. 6. Fox PT, Burton H, Raichle M. Mapping human somatosensory cortex with positron emission tomography. J Neurosurg 1997;67:34-43. 7. Kim PE, Singh M. Functional magnetic resonance imaging for brain mapping in neurosurgery. Neurosurg Focus 2003;15:1-7. 8. Belliveau JW, Kennedy DN, Jr, McKinstry RC, Buchbinder BR, Weisskoff RM, Cohen MS, et al. Functional mapping of the human visual cortex by magnetic resonance imaging. Science 1991;254:716-19. 9. Ogawa S, Lee TM, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 1990;87:9868-72.

Functional MRI in image guided neurosurgery

10. Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, Merkle H, et al. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA 1992;89:5951-5. 11. Fox PT, Raichle ME. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc Natl Acad Sci USA 1986;83:1140-4. 12. Iadecola C. Regulation of the cerebral microcirculation during neural activity: is nitric oxide the missing link? Trends Neurosci 1993;16:206-14. 13. Bandettini PA, Wong C, Hinks RS, Tifosky RS, Hyde JS. Time course EPI of human brain function during task activation. Magn Reson Med 1992;25:390-7. 14. Rees G, Friston K, Koch C. A direct quantitative relationship between the functional properties of human and macaque V5. Nat Neurosci 2000;3:716-23. 15. Heeger DJ, Huk AC, Geisler WS, Albrecht DG. Spikes versus BOLD: what does neuroimaging tell us about neuronal activity? Nat Neurosci 2000;3:631-3. 16. Connelly A, Jackson GD, Frackowiak RS, Belliveau JW, Vargha-Khadem F, Gadian DG. Functional mapping of activated human primary cortex with a clinical MR imaging system. Radiology 1993;188:125-30. 17. Stehling MK, Turner R, Mansfield P. Echo-planar imaging: magnetic resonance imaging in a fraction of a second. Science 1991;254:43-50. 18. Cosgrove GR, Buchbinder BR. Functional MRI for planning cortical resections. In: Alexander E, Maciunas R, editors. Advanced neurosurgical navigation. New York: Thieme; 1997. 19. Roux FE, Ibarrrola D, Tremoulet M, Lazorthes Y, Henry P, Sol JC, et al. Technical and methodological issues for integrating functional MRI in a neuronavigational system. Neurosurgery 2001;49:1145-57. 20. Gore JC. Principles and practice of functional MRI of the human brain. J Clin Invest 2003;112:4-9. 21. Detre JA. fMRI: applications in epilepsy. Epilepsia2004;45 Suppl 4:26-31. 22. Lee CC, Ward HA, Sharbrough FW, Meyer FB, Marsh WR, Raffel C, et al. Assessment of functional MR imaging in neurosurgical planning. Am J Neuroradiol 1999;20: 1511-19. 23. Wilkinson ID, Romanowski CA, Jellinek DA, Morris J, Griffiths PD. Motor functional MRI for pre-operative and intraoperative neurosurgical guidance. Br J Radiol 2003;76:98-103. 24. Elster AD, Burdette JH. Questions and answers in magnetic resonance imaging. 2nd ed. St. Louis: Mosby; 2001. p. 273-80. 25. Binder JR, Swanson SJ, Hammeke TA, Morris GL, Mueller WM, Fischer M, et al. Determination of language dominance using functional MRI: a comparison with the Wada test. Neurology 1996;46:978-84.

20

26. Herholz K, Reulen HJ, von Stockhausen HM, Thiel A, Ilmberger J, Kessler J, et al. Preoperative activation and intraoperative stimulation of language-related areas in patients with glioma. Neurosurgery 1997;41:1253-60. 27. Hinke RM, Yu X, Stillman AE, Kim SG, Merkle H, Salmi R, et al. Functional magnetic resonance imaging of Broca’s area during internal speech. Neuroreport 1993;4:675-8. 28. Hirsch J, Ruge MI, Kim KH, Correa DD, Victor JD, Relkin NR, et al. An integrated functional magnetic resonance imaging procedure for preoperative mapping of cortical areas associated with tactile, motor, language, and visual functions. Neurosurgery 2000;47:711-21. 29. Ruge MI, Victor J, Hosain S, Correa DD, Relkin NR, Tabar V, et al. Concordance between functional magnetic resonance imaging and intraoperative language mapping. Stereotact Funct Neurosurg 1999;72:95-102. 30. Fandino J, Kollias SS, Wieser HG, Valavanis A, Yonekawa Y. Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex. J Neurosurg 1999;91:238-50. 31. Jack CR, Jr, Thompson RM, Butts RK, Sharbrough FW, Kelly PJ, Hanson DP, et al. Sensory motor cortex: correlation of presurgical mapping with functional MR imaging and invasive cortical mapping. Radiology 1994;190:85-92. 32. Lehe´ricy S, Duffau H, Cornu P, Capelle L, Pidoux B, Carpentier A, et al. Correspondence between functional magnetic resonance imaging somatotopy and individual brain anatomy of the central region: comparison with intraoperative stimulation in patients with brain tumors. J Neurosurg 2000;92:589-98. 33. Puce A, Constable RT, Luby ML, McCarthy G, Nobre AC, Spencer DD, et al. Functional magnetic resonance imaging of sensory and motor cortex: comparison with electrophysiological localization. J Neurosurg 1995;83: 262-70. 34. Yetkin FZ, Mueller WM, Morris GL, McAuliffe TL, Ulmer JL, Cox RW, et al. Functional MR activation correlated with intraoperative cortical mapping. Am J Neuroradiol 1997;18:1311-15. 35. Majos A, Tybor K, Stefan´czyk L, Go´raj B. Cortical mapping by functional magnetic resonance imaging in patients with brain tumors. Eur Radiol 2005;15:1148-58. 36. Roux FE, Boulanouar K, Ranjeva JP, Tremoulet M, Henry P, Manelfe C, et al. Usefulness of motor functional MRI correlated to cortical mapping in Rolandic low-grade astrocytomas. Acta Neurochir (Wien) 1999;141:71-9. 37. Yousry TA, Schmid UD, Jassoy AG, Schmidt D, Eisner WE, Reulen HJ, et al. Topography of the cortical motor hand area: prospective study with functional MR imaging and direct motor mapping at surgery. Radiology 1995;195:23-9. 38. Mueller WM, Yetkin FZ, Hammeke TA, Morris GL, III, Swanson SJ, Reichert K, et al. Functional magnetic

297

298

20 39.

40.

41.

42.

43.

44. 45.

46.

47.

48.

49.

50.

51.

Functional MRI in image guided neurosurgery

resonance imaging mapping of the motor cortex in patients with cerebral tumors. Neurosurgery 1996;39:515-20. Schudler M, Maldijian JA, Liu WC. Functional imagedguided surgery of intracranial tumors located in or near the sensorimotor cortex. J Neurosurg 1998;83:412-18. Boling W, Parsons M, Kraszpulski M, Cantrell C, Puce A. Whole-hand sensorimotor area: cortical stimulation localization and correlation with functional magnetic resonance imaging. J Neurosurg 2008;108:491-500. Brannen JH, Badie B, Moritz CH, Quigley M, Meyerand ME, Haughton VM. Reliability of functional MR imaging with word-generation tasks for mapping Broca’s area. Am J Neuroradiol. 2001;22:1711-18. FitzGerald DB, Cosgrove GR, Ronner S, Jiang H, Buchbinder BR, Belliveau JW, et al. Location of language in the cortex: a comparison between functional MR imaging and electrocortical stimulation. Am J Neuroradiol 1997;18:1529-39. Roux FE, Boulanouar K, Lotterie J-A, Mejdoubi M, LeSage JP, Berry I. Language functional magnetic resonance imagine in preoperative assessment of language areas: correlation with direct cortical stimulation. Neurosurgery 2003;52:1335-45. McKhann GM, II, Hirsch J. Comment on reference 43. Neurosurgery 2003;52:1346. Petrovich N, Holodny AI, Tabar V, Correa DD, Hirsch J, Gutin PH, et al. Discordance between functional magnetic resonance imaging during silent speech tasks and intraoperative speech arrest. J Neurosurg 2005;103:267-74. Kombos T, Suess O, Kern BC, Funk T, Hoell T, Kopetsch O, et al. Comparison between monopolar and bipolar electrical stimulation of the motor cortex. Acta Neurochir (Wien) 1999;141:1295-301. Yoo SS, Talos IF, Golby AJ, Black PM, Panych LP. Evaluating requirements for spatial resolution of fMRI for neurosurgical planning. Hum Brain Mapp 2004;21:34-43. Sabbah P, Foehrenbach H, Dutertre G, Nioche C, DeDreuille O, Bellegou N, et al. Multimodal anatomic, functional, and metabolic brain imaging for tumor resection. Clin Imaging 2002;26:6-12. Archip N, Clatz O, Whalen S, Kacher D, Fedorov A, Kot A, et al. Non-rigid alignment of pre-operative MRI, fMRI, and DT-MRI with intra-operative MRI for enhanced visualization and navigation in image-guided neurosurgery. Neuroimage 2007;35:609-24. Gati JS, Menon RS, Ugurbil K, Rutt BK. Experimental determination of the BOLD field strength dependence in vessels and tissue. Magn Reson Med 1997;38: 296-302. Rugg MD, Johnson JD, Park H, Uncapher MR. Encoding-retrieval overlap in human episodic memory: a functional neuroimaging perspective. Prog Brain Res 2008;169:339-52.

Imaging in Stereotactic Surgery

17 General Imaging Modalities: Basic Principles A. A. Gorgulho . W. Ishida . A. A. F. De Salles

Historical Landmarks and Principles Although not based on imaging, the basic principle of stereotactic surgery started with the work of Zernov in 1890 [1]. A Russian anatomist, he developed a map of the brain cortex depicted in a hemisphere that, when attached to the human head, would keep a constant relationship with corresponding functional areas of the cortex. This instrument allowed placement of the craniotomy guided by the patient’s symptoms [2]. Further studies of the function of the central nervous system and symptoms the diseases required a more precise approach than the one devised by Zernov. Precise placement of recording and stimulating electrodes in specific areas of the brain to unveil function of deep structures called for a mathematical approach, Horsley and Clark devised and reported it in 1906 [3]. The Cartesian coordinate system, X (lateral), Y (anterior-posterior), Z (cranial-caudal), was born and remains the basis of stereotactic surgery (> Figure 17-1). If one reads the original work of Horsley and Clark, a striking finding is seen to the modern eyes; no imaging is mentioned for targeting the deep structures of the brain of the experimental animal [4]. As imaging was not readily available at the time, the skull landmarks were used as stereotactic reference. X-rays had just been described in Germany by Roentgen in 1895, only ten years before the seminal description of the stereotactic technique through the collaboration of the two English scientists, a surgeon and a physicist [3,4]. As the information age was not #

Springer-Verlag Berlin/Heidelberg 2009

as fast pace as it is today, years were necessary for the incorporation of scientific accomplishments to surgery. Although stereotactic surgery continued to be largely employed in the laboratory, using the Horsley and Clark’s interaural line and midline as reference [5], these skull-based reference points were too variable to allow a safe determination of a target in the depth of the human brain [6]. Moreover, little was known about the function of the deep structures of the brain to allow intervention in humans. The natural path of animal experimentation was necessary for confirmation of the effects of lesioning of brain structures before one would propose interventions in humans. It was approximately 20 years after the initial studies of Horsley and Clark on the functional anatomy of the deep brain structures that the theory of basal ganglia motor integration was put forward by Spatz [7]. This theory spearheaded the first attempts of surgery in the extrapyramidal system to control movement disorder [8].

Ventriculography and the Stereotactic Landmarks Parallel to these animal laboratory experimentations, imaging of the brain was being developed. Plain skull x-rays were followed by the description of ventriculography by Dandy in 1918 [9] and by angiography in 1927 by Egas Muniz [10]. These two monumental imaging modalities would dominate the landscape of stereotactic surgery for the following 50 years, firmly

252

17

General imaging modalities: basic principles

. Figure 17-1 The Horsley and Clark stereotactic apparatus. Although the X, Y, Z coordinates’ convention changed over the years, modern convention is as follows: the ‘‘X’’, ‘‘Y’’, and ‘‘Z’’ are right-left, antero-posterior and cranio-caudal displacement from the stereotactic space center respectively. (These pictures are a courtesy of the historical collection at UCLA Medical Library. This is the second Horsley and Clark apparatus assembled in history)

establishing the association of imaging and stereotactic localization. Since then stereotactic surgery has developed in parallel with imaging techniques. Early in their work, Spiegel and Wycis realized the importance of the stereotactic technique for morphological and functional neurosurgical interventions [6]. They described the need for improved imaging for visualization of deep brain structures, and actually developed methods of determination of stereotactic coordinates based on the calcification of the pineal gland, lately based on pneumoencephalography. The posterior commissure-pons line served as reference for their measurements. These measurements were used mainly for functional stereotactic surgery. While the development of functional stereotactic surgery was rapid with the perfection of their stereotactic frame (> Figure 17-2), the morphological applications evolved slowly because the visualization of lesions in the brain became available only with the incorporation of angiography to the stereotactic technique. Although few neurosurgeons still use ventriculography for functional neurosurgery, its use is practically a historical legacy.

. Figure 17-2 Spiegel and Wycis stereotactic device constructed in 1954, available at University of California in Los Angeles. As in Figure 19-1 notice the Cartesian coordinates, X, Y, and Z applied to human stereotactic surgery

General imaging modalities: basic principles

The main legacy of ventriculography and pneumoencephalography in stereotoactic surgery is the anterior-commissure (AC) and posteriorcommissure (PC) line. AC is seen approximately 2 mm below the posterior border of the foramen of Monro, while PC is seen just cranial to the entrance of the aqueduct of Sylvius and just caudal to the pineal calcification. These two anatomical landmarks, now readily visualized on all plans of the MRI, specifically seen in the sagittal and axial plan [> Figure 17-3], supported the development of the main atlases of the human brain, Shaltelbrand and Wahren [11] and Talairach’s proportional atlas of the human brain [12]. Specific targets in the brain are described based on the distance of the midcommissural plane which is the intersection of the

17

Cartesian coordinates dividing the brain into eight quadrants. Talairach used the length of the AC-PC line to develop the proportional atlas of the human brain widely used in epilepsy surgery.

Angiography Angiography paralleled the developments in stereotactic surgery. Stereotactic angiography was introduced by Talairach’s group [13]. Those workers dedicated several years of research to developing safe methods of inserting recording electrodes and radioisotope-loaded catheters and mapping the cortical anatomy by means of angiography. Their pioneer work using orthogonal

. Figure 17-3 T1 MRI axial and sagittal sections passing through AC-PC planes. (a) and (b) are axial AC-PC planes, in (a) without correction for AC-PC plane angle, notice the arrows showing AC (upper arrow) and PC (lower arrow). (b) shows the MRI precisely at AC-PC axial plane as reconstructed by the stereotactic software. (c) and (d) are sagittal AC-PC planes, in (c) without correction to the horizontal plane, notice the arrows AC (left arrow) and PC (right arrow). (d) shows AC-PC aligned to the horizontal plane by the stereotactic software

253

254

17

General imaging modalities: basic principles

approach to avoid the cerebral vasculature in functional and tumor stereotaxis established the grounds for several groups to use stereotactic angiography [14]. Specially trained neurosurgeons dedicated to epilepsy surgery followed Talairach’s work. Techniques of angiography mapping of the brain promptly brought to computerized stereotaxis, initially through the use of superimposition techniques [15,16], later by digitization or scanning of angiographic films [17], and more recently in DICOM format, even with three dimensional angiography [18]. Talairach’s group also concentrated on the understanding of the three-dimensional (3D) characteristics of the cerebral vasculature and its relationship with cerebral tumors aiming to develop diagnostic and therapeutic approaches, either with precisely placed craniotomy or by the use of stereotactic-guided placement of isotopes [14,19]. Because of the inherent two-dimensional nature of angiography, they relied on stereoscopic techniques to obtain the 3D information. The knowledge developed with stereotactic angiography led to the treatment of arteriovenous malformation (AVMs) with single dose radiation [20]. Angiography was not widely married with the stereotactic technique to approach intracranial lesions until the application of stereotactic radiosurgery for AVMs was described in 1972 [20]. Talairach described the implantation of isotopes for treatment of subcortical tumors using the blush of the angiogram [14], and Leksell described the use of external beam radiation directed stereotactically to obliterate intracranial targets and coined the term ‘‘Radiosurgery’’ [21]. Diagnostic procedures using the stereotactic technique were initiated only a decade later, despite the poor and only indirect visualization of structural brain lesions [22,23]. The number of morphological procedures surpassed the functional applications of stereotactic surgery with the advent of computed-imaging techniques which allowed direct visualization of

the target [24]. Angiography sponsored the fast development of radiosurgery and approaches for determination of the seizure foci in epilepsy surgery.

Computerized Era When computed tomography (CT) scan became available to stereotactic surgery, approximately 30 years after the first human stereotactic proedure, stereotactic surgery had a second revolution [24]. Now lesions could be visualized and the risk of approaching highly vascularized lesions became measurable. Biopsies of brain tumors, brachytherapy and especially radiosurgery dominated the time of stereotactic surgeons during the 1980s and 1990s [25]. CT scan also brought back the interest of neurosurgeons to lesioning the depth of the brain for symptom control in neurodegenerative disease such as Parkinson’s disease, since the precision and the safety of the stereotactic method improved [26]. The functional stereotactic landmarks well seen in Dandy’s ventriculography, which served the bases for all the electrophysiological studies of the specialty, were now well seen with the CT scan. The 1980s saw the resurrection of lesioning in the brain as a therapeutic option. The ventriculographic approach was compared with the computerized approach and the computerized era for functional neurosurgery was established [27]. However it was the morphological application of the stereotactic method that spearheaded this revolution and extension of the technique to common place in the regular operating room of the general neurosurgeon [28]. This came with the progressive abandonment of the stereotactic frame for image-guided surgery using triangulation methods and explosion of stereotactic radiosurgery as a minimally invasive technique for treatment of brain tumors and arteriovenous malformations [29,30].

General imaging modalities: basic principles

Computer Tomography Stereotactic Principles Hounsfield rightly received the Nobel Prize for medicine in 1979 for his description of X-Ray computed tomography (CT) in 1973 [31]. The imaging modality revolutionized neuroscience and the knowledge of brain pathology, function, and the ability of the stereotactic neurosurgeon to approach the brain safely. The technique was developed for visualization and not for precise calculation of intracranial targets. Therefore, years of work of stereotactic surgeons was necessary to bring this image safely into stereotactic surgery. As CT provided axial images only, stereotactic surgeons could determine only two coordinates from the slice of interest, i.e., where the target was located, either the pathology or the functional site to be targeted. By convention, the ‘‘X’’ became the lateral coordinate and the ‘‘Y’’ the antero-posterior. The vertical coordinate was not seen in the chosen slice, and the stereotactic surgeon had to devise methods of ‘‘Z’’ determination. Initially stereotactic surgeons relied upon the movement of the CT scan table to calculate the ‘‘Z’’, however the manufacturers of the CT scans were not worried about the precision of movement of the table, since the scanners were built for diagnosis. Frames were developed to overcome this imprecise movement of the table. The best example of such strategies is the Laitinen’s device which had transverse bars calibrated to correct the imprecision of the table movements [32]. It was not until the clever oblique bar introduced to a localizing box attached to the stereotactic frame by a graduate student at the University of Utah that the problem of the ‘‘Z’’ coordinate could be solved (> Figure 17-4) [33]. The stereotactic frame with the localization box became standard for all stereotactic procedures, including functional and morphological, from fine lesioning of pathways in the brain, to

17

. Figure 17-4 Axial representation of the fiduciary system with explanation of the oblique fiducial of the stereotactic localizing box. The Brown-Roberts-Wells (BRW) localizing box allows for three-dimensional definition of a point in any imaging slice (insert). The 9 points fiduciary system became widely used because of the possibility to correct for frame misaligment. The X and Y can be directly extracted from the axial slices, while the Z is calculated using the distance between the oblique bar to the reference bar in each slice

implanting electrodes to biopsies and craniotomy [16,34]. All commercially available stereotactic frames were adapted for the use of the oblique fiducials for determination of the ‘‘Z’’ (vertical) coordinate. The accuracy of the method was compared to the most used frames and shown to be submillimetric [35]. CT is considered up to now the most precise method for determination of stereotactic coordinates. The nature of X-rays with its rectilinear path avoids the introduction of distortions in the calculations. Distortions are introduced when using magnetic resonance imaging (MRI).

MRI Principles As the MRI scan became available and its geometric distortions were controlled [36–38], this imaging technique was preferred by stereotactic

255

256

17

General imaging modalities: basic principles

surgeons [39,40]. Because it presents exquisite visualization of the nuances of the brain pathways and nuclei and the consequences of the surgery [41–43], it has revolutionized the approach of functional stereotactic surgery, no longer depending so much on ventricular landmarks, but relying on direct targeting of the structure needing functional modification [44]. Brain-function visualization is the next frontier on the development of stereotactic targeting. The incorporation of the chronic electrical stimulation as a therapeutic approach, initially for treatment of behavioral disorders, then for refractory chronic pain and movement disorders and more recently again for psychiatric disorders, has decreased the serious complications of the approaches in the depth of the brain. Progressively lesions of nuclei and pathways are being replaced by the ability of electrical stimulation to modify function by focally modulating neurons and brain networks. Functional imaging becomes more important for modulation of functional diseases of the brain, such as the neurodegenerative disease, genetic pathologies and brain damage by ischemic or traumatic injuries. Functional MRI and the ability to operate inside the magnet using frame [39,41] or frameless techniques brought new opportunities for functional neurosurgery [45–47]. In the arena of morphologic stereotaxis the revolution was on imaging localization of tumors and malformations in the brain needing intervention. Initially stereotactic surgery was used for simple needle biopsy [48], then to aid resections and guidance [16]. Here also functional imaging and the exclusive visualization of fibers related to lesions are revolutionizing surgical resections and targeting functional stereotactic surgery (> Figure 17-5) [49,50]. These important imaging developments are readily applicable to stereotactic radiosurgery (SRS), currently representing substantial, if not the major application of the stereotactic technique [51]. Initially SRS

was dependent on the stereotactic frame [52] and now, similar to surgical resection, it is becoming independent of the frame approach [53].

Positron Emission Tomography and Stereotactic Procedures CT and MRI scans sometimes do not adequately demonstrate the regions of interest for the stereotactic procedures. Molecular imaging, capable of demonstrating pathologies not seen in morphologic imaging can complement the needs of stereotactic surgery. Positron emission tomography (PET) adds this important metabolic information, and when incorporated by fusion with CT and MRI, may allow more accurate targeting and treatment planning in stereotactic radiosurgery, tumor resection, and biopsy.

PET in Morphological Stereotactic Surgery Most PET scans use a radiotracer made up of a common metabolite, such as glucose or an amino acid, attached to a radioisotope such as 18F (Fluorine) or 11C (Carbon). The 18F-FDG (fluoro-deoxy-glucose) PET is most widely used, and when combined with CTor MRI, will demonstrate with exquisite anatomic precision regions of increased glucose metabolism. Since neoplasms and inflammatory lesions often have high glucose uptake matching that of the brain, differentiation of a lesion from normal surrounding brain may be limited. The amino acids, however, are selectively more utilized by neoplasms than normal brain. The 18F-DOPA (fluoro-phenylalanine) and 11C (Carbon) methionine PET scans utilize amino acid molecules, and have demonstrated increased radioactivity in neoplasms, when compared to normal brain [54,55]. Extent of surgical resection or radiosurgery targeting will sometimes

General imaging modalities: basic principles

17

. Figure 17-5 3-D frame and fiber tracking of the pyramidal system used for subthalamic nucleus targeting (traced arrow). Notice the distortions that can happen in fiducial system of the stereotactic localizing box (full arrows), reconstruction with iPlan software (BrainLab, Germany). This is a Leksell frame with copper sulfide liquid in the fiducial system (Elekta, Sweden)

be modified significantly by incorporation of PET on CT and MRI imaging [56–58]. Fluorodopa PET, C-methionine PET, and other amino acid-based PET scans have proven to be more effective than FDG-PET for imaging of neoplasms [54,59]. Fluorodopa and C-methionine PETscans demonstrated sensitivity to low grade as well as high grade tumors, and may help to differentiate areas of radiation necrosis (> Figure 17-6) [59,60]. PET scans sometimes demonstrate evidence of tumor recurrence before CT or MRI. They have proven to be most helpful in the management of gliomas [56–58], but also useful in treatment of other malignancies. It can be of help with pituitary adenomas [61], meningiomas, and parasellar lesions, where proximity to the cavernous sinus makes differentiation of tumor

from normally enhancing structures difficult. PET has proven to be helpful with spinal cord tumors [62,63], particularly in the presence of instrumentation or in the patient not able to tolerate MRI (pacemaker or electrical stimulator) in preparation for radiosurgery.

PET Scans in Functional Neurosurgery The PET characteristics of brain anatomy under normal and abnormal conditions have provided clues to a better understanding of brain anatomy and physiology. Changes on PET scanning related to deep brain stimulation have added to the still rudimentary body of information relating

257

258

17

General imaging modalities: basic principles

. Figure 17-6 Fluorodopa-PET to differentiate tumor recurrence from radiation necrosis. Nonsmall cell carcinoma brain metastasis treated with radiosurgery using 16 Gy prescribed to the 90% isodose line. (a) T1 MRI with gadolinium showing lesion growth with central hypo-intensity, possibly radiation necrosis. (b) Fluorodopa PET performed one year after the treatment and at the same time of the MRI in (a). (c) Coronal PET showing higher uptake of Fluorodopa in the lesion (full arrow) than in the basal ganglia (traced arrow), consistent with tumor recurrence. Histology of the resected specimen showed nonsmall cell carcinoma with focal necrosis

to pain, movement disorders, and behavioral problems. The noninvasiveness of PET makes it a valuable research modality. Striatal as well as extra-striatal dopaminergic activity in neurological and psychiatric disorders have been studied using PET biomarkers [64]. The PET tracers are very important in advanced research on problems of early and more specific diagnosis of major movement and psychiatric disorders, physiology of the dopaminergic system, evolution of disease processes, and response to medications and surgical interventions [65–68]. FDG-PET studies in patients with major depression have demonstrated increased glucose metabolism in the left amygdala and frontal limbic pathways, with evidence of decreased amygdala metabolism under antidepressant drug treatment [69] and/or vagus nerve stimulation [70]. Similar PET responses have been reported with deep brain stimulation of the anterior limbic system, such as the subcallosal cingulate gyrus [71]. These findings are consistent with the findings of PET blood flow studies in depressed patients by Mayberg et al. [72,73]. Mayberg et al. used the findings of increased blood flow in the sub-genual cingulate cortex, area AcG25, to realize a target

for deep brain stimulation to control the symptoms of medically refractory major depression. Mayberg et al’s early work demonstrated the integral role played by the subgenual cingulate cortex in both, normal, and pathological shifts in mood [73]. Increases in limbic and paralimbic blood flow (as measured using PET) occur in the subgenual cingulate cortex and anterior insula during sadness. There is a significant inverse correlation between blood flow in the subgenual cingulate cortex and right dorsolateral prefrontal cortex [74]. A clinical response to antidepressants is associated with limbic and striatal (subgenual cingulate cortex, hippocampus, insula, and pallidum) decreases in metabolism and dorsal cortical (prefrontal, parietal, anterior, and posterior cingulate cortex) increases in metabolism [69,72]. In 2005, DBS electrodes were bilaterally implanted in the subgenual cingulate cortex [75] of 6 patients with medically refractory major depression. When stimulation was on, patients reported positive emotional phenomena. In the acute postoperative period the patients experienced reproducible increases in activity and mood scores, changes that failed to occur during sham stimulation. Chronic stimulation at high

General imaging modalities: basic principles

frequency, probably leading to suppression of function in the site, resulted in significant response and remission of depression in 4 of the 6 patients at 6 months. These well conducted studies showed the effectiveness of PET findings to enhance the knowledge of brain function leading to diagnosis and therapeutic measures. Anterior capsule deep brain stimulation has resulted in decreased (18) FDG-PET activity or decreased glucose uptake in the subgenual anterior cingulate gyrus and ventral striatum in a group of patients with refractory obsessive compulsive disorder [76]. OCD patients with hoarding behavior showed different patterns of cortical PET- FDG activity, compared to those with nonhoarding behavior [77]. Evidence is accumulating to support the use of PET in routine target determination and follow up of patients undergoing neurosurgical interventions for mental illness. Advances in radioligand technology [78] have provided radioisotope labeled molecules that enable study of neurotransmitters (serotonin, norepinepherine, dopamine and glutamate) and their receptors with PET [79–82]. Patterns and intensity of uptake have added to our understanding of movement and psychological disorders. As an example fluorodopa-PET uptake in the putamen would be decreased in idiopathic Parkinson’s Disease as well as in a Parkinson’s-Plus condition. However, greater loss of striatal D2 receptors in Parkinson’s-Plus on a (11)C-raclopride PET scan might help to identify the patient as being unsuitable for surgical treatment with stereotactic implant of DBS, pallidal or thalamic lesion. Radioligands and PET have advanced the study of neuroreceptors remaining a most valuable tool for ongoing studies and treatment of patients with motor and psychological disorders [83].

Image Fusion The ability to bring multimodality imaging to plan stereotactic procedures started with the work of Talairach. He obtaining information

17

from angiography to avoid vasculature for seizure placement of electroencephalographic electrodes for seizure focus determination [13]. The attempt to bring MRI and CT into the stereotactic space determined by plain X-ray was started for stereotactic radiosurgery with fusion of imaging by photographic magnification manipulation [15]. These efforts have culminated with computerized fusion with software algorithms developed based on contours, image intensity, and voxel matching. These precise approaches have allowed gathering detailed information prior to the procedure, facilitating the surgery planning. Before these techniques were available, the patient had imaging with the stereotactic frame in place and multimodality approaches were unyielding. Now a portable CT scan in the operating room has obviated the need of elaborate stereotactic operating rooms. The fusion techniques offer also the opportunity of atlas information integration to the patient’s image (> Figure 17-7). Moreover, real time information on brain shift and possible complication during the operation are obtained while operating inside the magnet [39,41]. Fusion of multimodality images is very important for correction of distortions of PET, digital angiography and MRI scans. The portable CT in the operating room can offer this correction [38,84].

Image-Guided Surgery The integration of multimodality imaging is possible without the stereotactic frame [85–87]. This capability has revolutionized not only stereotactic surgery but also general neurosurgery. It is now impacting in other specialties such as radiation oncology, orthopedic surgery, head and neck surgery and general surgery. Modern imaging technology brings presurgical information to the surgeon that obviates unknowns. Computer technology, using this information, provides that surgery can be performed virtually on a screen before the patient is even touched. In addition, surgery has advanced to a level

259

260

17

General imaging modalities: basic principles

. Figure 17-7 (A) Shaltenbrand-Wahren coronal plate. (B) Superimposition of the anatomy in (A) onto the corresponding MRI coronal slice by iPlan stereotactic software (BrainLab, Germany). Notice the adjusting sliding scale under (A) capable of matching the atlas with the MRI

where minimal invasion and maximal effectiveness is routine. The term ‘guided surgery’ in the modern sense, should be viewed as ‘modern surgery’. Guided surgery’, however, is still seen by many as the use of computerized imaging, or traditional X-ray-based stereotactic techniques described above to bring the surgeon precisely to the pathology being operated on. The pressures of competition and multimillion dollar malpractice law suits have driven the modern medical centers to invest heavily in technology. This in turn has driven the price of medical procedures to almost unacceptable levels. The

hope is that applied technology can decrease the costs of each patient treatment. Image guided surgery is an area that may lead to substantial savings in medical dollars. The scope of the approaches and the realistic surgical undertaking may lead to shorter hospital stays due to fewer complications related to extensive surgeries, less need for long convalescent and rehabilitation periods, and, consequently, a faster return of the patient to the workforce. Ultimately, this results in decreasing the overall price of medical care. This concept has been exemplified with complex skull base disease.

General imaging modalities: basic principles

These difficult tumors are treated now with transnasal procedures for skull base tumor resections [88] under real time imaging in the operating room, and followed by radiosurgery, reducing patient recovery time, decreasing morbidity, and offering the patient complete control of their disease [89]. The stereotactic developments throughout the 20th century as described in this chapter, spearheaded by the computerized imaging, provided remarkable noninvasive imaging techniques developed primarily for diagnostic studies. These techniques were adapted for surgery guidance with navigation using triangulation techniques [85–87]. Now infrared reflectors or magnetic field are used for real-time localization [90]. Fast computers and smart software packages permitted the introduction of these images to the operating field to guide the surgeon. Digital fluoros copy, ultrasound, computer tomography (CT), magnetic resonance imaging (MRI) and positron emission tomography (PET) are now brought to the operating room and combined with merging data set techniques, allowing the surgeon to take advantage of a wealth of information that was previously unavailable. The surgeons of the past relied upon the principle of ‘‘exposure, exposure, exposure’’, and their individual knowledge of gross anatomy to perform surgery. The surgeons of the present rely on their knowledge of anatomy, anatomical imaging, and functional anatomy to perform minimally invasive procedures and solve previously unapproachable problems [91].

Spine Stereotactic Surgery Invasive stereotactic fixation for radiosurgery of the spine was previously tried without acceptance from the stereotactic community [96]. The procedure proved to be too invasive and impractical to be largely applied. The development of imageguided surgery, as described above, provided the

17

base for the development of the spine stereotactic technique. Image fusion and computerized image are now applied to stereotactic radiosurgery of spine lesions [91,94,95] and for placement of hardware. Completely noninvasive, fiducial systems use infrared triangulation and online image fusion of oblique X-rays and CT reconstruction to provide real-time movement tracking and targeting of lesions in the spine and surrounding regions [97,98]. The technology has reached precision to treat intramedullary lesions (> Figure 17-8).

Future Directions We are on the verge of perfecting real-time imaging in surgery [39,46]. During the past decade, the information brought during surgery by plain X-rays, fluoroscopy, and ultrasound was maximized and their limitations were established. Surgeons have now turned their eyes to the wealth of possibilities brought by portable CT scans and operating rooms equipped with interventional MRIs. MRI offers the possibility of not only exquisite anatomical information during surgery, but also dynamic changes of this anatomy associated with real-time changes in function. It also carries the advantage of not being harmful to the medical personnel, as are techniques dependent on isotopes or X-rays. The operating room with multimodality imaging, also known as operating room of the future, is a focus of studies in major medical centers. The logistics and real advantages of bringing a complex technology such as MRI to the operating room, or bringing the operating room to the complex MRI environment, has become a subject of symposiums on modern surgery [41]. The evolving field of functional MRI has brought the possibility of deciding before surgery the location of a fine function in the brain in relation to pathology (> Figure 17-9). It has also allowed relating the complex wiring of the brain to the location of ‘brain pace makers’ (> Figure 17-5

261

262

17

General imaging modalities: basic principles

. Figure 17-8 Medullary AVM in a 22-year-old woman who bled, developed tetraplegia and recovered after a C2–C7 laminectomy. (a) Sagittal contrasted T1 MRI before radiosurgery. (b) Sagittal CT with the radiosurgery plan (12 Gy, 90% isodose line, 1.60 cc lesion). (c) Sagittal contrasted T1 MRI 24-months post-radiosurgery. (d) Anteroposterior angiogram before treatment, notice the angiographic stereotactic fiducials (traced arrow). (e) Coronal CT showing the radiosurgery plan. (f) Anteroposterior angiogram post-treatment. Full arrows point the initial nidus (a), residual at 24 months (c) and residual at 26 months (f)

and > Figure 17-10). All this information is readily related to imaging during surgery. Products that integrate information from multiple imaging sources with diffusion of fluids through tissues, such as brain parenchyma for delivery of drugs after resection, have started to appeart on the market. This is achieved with stereotactic precision. Similar information is being generated by therapeutic thermal application, electrical current, and radiation. Laser or radiofrequency ablation, electrical stimulation with smart pacemakers capable of receiving and analyzing physiological clues, and radiation delivery with

modulating capabilities are all novel approaches being developed [92,93]. The operating room of the future for ‘guided surgery’ and modern stereotactic surgery, requires real-time anatomical imaging technology related to function of the tissue under therapy at the moment of resection, lesioning or modulation [42,93]. This allows maximization of resection, drug infusion, electrical tissue influence, biopsy and the optimal use of radiation strategies to manipulate biological systems [92,101]. The patient should be least invaded and most helped by the modern stereotactic techniques.

General imaging modalities: basic principles

17

. Figure 17-9 (a) Functional MRI showing Broca’s area (traced arrows) just posterior to an Arteriovenous Malformation (full arrows). The same AVM is shown on anteroposterior (b) and oblique (c) angiogram. The AVM removed through a craniotomy guided by stereotactic triangulation with the patient awake for complete speech preservation, lateral angiogram (d)

. Figure 17-10 MRI fiber tracking from the subgeneal area (AcG25) recognized as the stereotactic target for implantation of deep brain stimulation electrodes for treatment of medically refractory depression, Notice the virtual electrode placement (open arrows). Notice the fibers going to prefrontal and orbitofrontal cortex and cingulate fasciculus (full arrows) [49,50]. (a) shows 3-D, sagittal and coronal reconstructions with axial MRI passing through posterior commissure, (b) same reconstruction passing through anterior commissure (traced arrows)

263

264

17

General imaging modalities: basic principles

References 1. Zernov DN. L’ence´phalome´tre. Rev Gen Clin Ther 1890;19:302. 2. Kandel EI, Schavinsky YV. Stereotaxic apparatus and operations in Russia in the 19th century. J Neurosurg 1972;37:407-411. 3. Clark RH, Horsley V. On a method of investigating the deep ganglia and tracts of the central nervous system (cerebellum). Brit Med Journal 1906;2:1799-1800. 4. Horsley V, Clark RH. The structure and function of the cerebellum examined by a new method. Brain 1908;31:45-125. 5. Sun B, De Salles AAF, Medin P, Solberg T, Hoebel B, Felder-Allen M, Wie C-W, Ackerman R. Reduction of hippocampal-kindled seizure activity in rats by stereotactic radiosurgery.Experimental Neurology. 1998;154:691-695. 6. Spiegel EA, Wycis HT. Stereoencephalotomy, Part I. New York: Grune & Stratton; 1952. 7. Pia HW. In memory of Hugo Spatz 1888–1969. Acta Neurochir (Wien) 1970;23(2):183-6. 8. Gildenberg PL. Evolution of Basal Ganglia Surgery for Movement Disorders. Stereotact Funct Neurosurg 2006;84:131-135. 9. Dandy WE. Ventnculography following the injection of air into the cerebral ventricles. Ann Surg 1918;68:5-11. 10. Moniz E, de Carvalho L, Almeida Lima P. Angiopneumographie. Presse Med 1931;39:996-999. 11. Schaltenbrand G, Wahren AE. Stereotaxy of the human brain. Stuttgart: Thieme; 1982. 12. Talairach J, David M, Tournoux P, Corredor H, Kvasina T. Atlas d’anatomie stereotaxique. Paris: Masson; 1957. 13. Szikla G, Bouvier G, Hori T, et al. Angiography of the human brain cortex. Berlin: Springer-Verlag; 1977. 14. Talairach J, Aboulker P, Ruggiero G, et al. Utilization del methode radiostereotaxic pour le traitement radioactive in situ des tumeurs cerebrales. Rev Neurol 1953;90:656-658. 15. De Salles AAF, Asfora WT, Abe M, Kjellberg RN. Transposition of target information from the magnetic and computed tomography scan images to conventional X-ray stereotactic space. Appl Neurophyisol 1987;50:23-32. 16. Kelly PJ. Tumor Stereotaxis. Philadelphia: Sounders; 1991. p. 108-113. 17. Zhang J, Levesque MF, Wilson CL, et al. Multimodality imaging of brain structures for stereotactic radiosurgery. Radiology 1990;175:435-441. 18. Pedroso AG, De Salles AA, Tajik K, Golish R, Smith Z, Frighetto L, Solberg T, Cabatan-Awang C, Selch MT. Novalis Shaped Beam Radiosurgery of arteriovenous malformations. J Neurosurg 2004;101 Suppl 3:425-34. 19. Bancoud J, Morel P, Talairach J, et al. Interet de l’exploration functionelle stereotaxique dans la localization des lesions expansives. Rev Neurol (Paris) 1961;105: 219-220.

20. Steiner L, Leksell L, Greitz T, et al. Stereotactic radiosugery for cerebral arteriovenous malforations: Report of a case. Acta Chir Scand 1972;138:459-462. 21. Leksell L. The stereotactic method of radiosurgery of the brain. Acta Chir Scand. 1951;102:316-319. 22. Housepian EM, Pool JL. Application of stereotaxic methods to histochemical, electromicroscopic and electrophysiological studies of bran subcortical structures. Confin Neurol 1962;22:173-177. 23. Kalynaraman S, Gillingham FG. Stereotaxic biopsy. J Neurosurg 1964;21:854-858. 24. Gildenberg PL. The history of stereotactic neurosurgery. Neurosurg Clin N Am 1990;1(4):765-80. 25. De Salles AAF, Goetsch SJ (eds.). Stereotactic Surgery and Radiosurgery. Madison, Wisconsin: Medical Physics Publishing Corporation; 1993. p. 1-16. 26. Laitinen LV, Bergenheim AT, Hariz MI. Leksell’s posteroventral pallidotomhy in the treatment of Parkinson’s disease. J Neurosurg 1992;76(1):53-61. 27. Hariz MI, Bergenheim AT. A comparative study on ventriculographic and computerized tomography-guided determinations of brain target in functional stereotaxis. J Neurosurg 1990;73:565-571. 28. Lunsford LD. The genesis of neurosurgery and the evolution of the neurosurgical operative environment: Part 1–Prehistory to 2003. Neurosurgery 2003;52(6): 1512. 29. De Salles AAF, Lufkin R. Minimally Invasive Therapy of the Brain. Thieme Medical Publishers; pp 1–6, 1997. 30. Lunsford LD. Radiosurgery as a future part of neurosurgery. Mayo Clin Proc. 1999;74(1):101-3. 31. Hounsfield GN. Computerized transverse axial scanning (tomography). I. Description of system. Br J Radiol 1973;46:1016-1022. 32. Laitinen LV, Hariz MI. Multi-purpose stereoadapter. Appl Neurophysiol 1987;50(1–6):68-76. 33. Heilbrun MP, Roberts TS, Apuzzo ML, Wells TH Jr, Sabshin JK. Preliminary experience with BrownRoberts-Wells (BRW) computerized tomography stereotaxic guidance system. J Neurosurg 1983;59(2):217-22. 34. Hariz MI. Correlation between clinical outcome and size and site of the lesion in CT-guided thalamotomy and Pallidotomy. Stereotactic and Funct Neurosurg 1990;54 (55):172-185. 35. Maciunas RJ, Galloway RL Jr, Latimer J, et al. An independent application accuracy evaluation of stereotactic frame systems. Stereotactic and Funct Neurosurg 1992;58:103-107. 36. Maciunas RJ, Fitzpatrick JM, Gadamsetty S, Maurer CR Jr. A universal method for geometric correction of magnetic resonance images for stereotactic neurosurgery. Stereotact Funct Neurosurg 1996;66(1–3):137-40. 37. Burchiel KJ, Nguyen TT, Coombs BD, Szumoski J. MRI distortion and stereotactic neurosurgery using the Cosman-Roberts-Wells and Leksell frames. Stereotact Funct Neurosurg 1996;66(1–3):123-36.

General imaging modalities: basic principles

38. Alexander E 3rd, Kooy HM, van Herk M, Schwartz M, Barnes PD, Tarbell N, Mulkern RV, Holupka EJ, Loeffler JS. Magnetic resonance image-directed stereotactic neurosurgery: use of image fusion with computerized tomography to enhance spatial accuracy. J Neurosurg 1995;83(2):271-6. 39. De Salles AAF, Frighetto L, Behnke E, Sinha S, Bronstein J, Torres R, Subramanian I, Cabatan-Awang C, Frysinger R. Functional Neurosurgery in the MRI Environment. Minim Invasive Neurosurg. 2004;47 (5):284-9. 40. Starr PA, Christine CW, Theodosopoulos PV, Lindsey N, Byrd D, Mosley A, Marks WJ Jr. Implantation of deep brain stimulators into the subthalamic nucleus: technical approach and magnetic resonance imaging-verified lead locations. J Neurosurg 2002;97(2):370-87. 41. Lee WYM, De Salles AAF, Frighetto L, Torres R, Behnke E, Bronstein J. Imaging techniques and electrode fixation methods for deep brain stimulation: Intraoperative MRI 0.2 T, 1.5 T and fluoroscopy. Minimally Invasive Neurosurgery 2005;48:1-6. 42. De Salles AAF, Brekhus SD, De Souza EC, Behnke EJ, Farahani K, Anzai Y, Lufkin R. Early postoperative appearance of radiofrequency lesions on magnetic resonance imaging. Neurosurgery 1995;36 (May):932-936. 43. De Salles AAF. Role of stereotaxis in the treatment of cerebral palsy. J of Child Neurology 1996;11:S43-S50. 44. De Salles AAF, Hariz M. MRI Guided Pallidotomy. In: Rengachary SS, editor. Neurosurgical Operative Atlas, Volume 7, Williams & Wilkins, AANS; 1998. pp 141-148. 45. Martin AJ, Hall WA, Roark C, Starr PA, Larson PS, Truwit CL. Minimally invasive precision brain access using prospective stereotaxy and a trajectory guide. J Magn Reson Imaging 2008;27(4):737-43. 46. Larson PS, Richardson RM, Starr PA, Martin AJ. Magnetic resonance imaging of implanted deep brain stimulators: experience in a large series. Stereotact Funct Neurosurg 2008;86(2):92-100. 47. Holloway KL, Gaede SE, Starr PA, Rosenow JM, Ramakrishnan V, Henderson JM. Frameless stereotaxy using bone fiducial markers for deep brain stimulation. J Neurosurg 2005;103(3):404-13. 48. Hariz MI, Bergenheim AT, De Salles AAF, Rabow L, Trojanowski T. Percutaneous stereotactic brain tumor biopsy and cyst aspiration with a non-invasive frame. British Journal of Neurosurgery 1990;4:397-406. 49. Sedrak M, Gorgulho A, De Salles AF, Frew A, Behnke E, Ishida W, Klochkov T, Malkasian D. The role of modern imaging modalities on deep brain stimulation targeting for mental illness. Acta Neurochir Suppl 2008;101:3-7. 50. Hauptman JS, DeSalles AA, Espinoza R, Sedrak M, Ishida W. Potential surgical targets for deep brain stimulation in treatment-resistant depression. Neurosurg Focus. 2008;25(1):E3. 51. De Salles AA, Gorgulho AA, Selch M, De Marco J, Agazaryan N. Radiosurgery from the brain to the

52. 53.

54.

55.

56.

57.

58.

59.

60.

61.

62.

63.

64.

65. 66.

67.

17

spine: 20 years experience. Acta Neurochir Suppl 2008;101:163-8. Leksell L. A stereotaxic apparatus for intracerebral surgery. Acta Chir Scand 1951;102:316-319. Agazaryan N, Tenn SE, DeSalles AA, Selch MT. Imageguided radiosurgery for spinal tumors: methods, accuracy and patient intrafraction motion. Phys Med Biol 2008;21;53(6):1715-27. Becherer A, Karanikas G, Szabo M, et al. Brain tumour imaging with PET: a comparison between [18F] fluorodopa and [11C] methionine. Eur J Nucl Med Mol Imaging 2003;30:1561-1567. Chen W, Cloughesy T, Kamdar N, et al. Imaging Proliferation in Brain Tumors with 18F-FLT PET: Comparison with 18F-FDG. J Nucl Med 2005;46:945-952. Grosu A, Weber W, Astner S, et al. 11C-Methionine PET Improves the Target Volume Delineation of Meningiomas Treated with Stereotactic Fractionated Radiotherapy. Int J Radiat Oncol Biol Phys 2006;66:339-344. Pirotte B, Goldman S, Dewitte O, et al. Integrated positron emission and magnetic resonance imagingguided resection of brain tumors: a report of 103 consecutive procedures. J Neurosurg 2006;104:238-253. Singhal T, Narayanan T, Jain V, et al. 11C-L-Methionine Positron Emission Tomography in the Clinical Management of Cerebral Gliomas. Mol Imaging Biol. 2008;10 (1):1-18. Chen W, Silverman D, Delaloye S, et al. 18 F-DOPA PET Imaging of Brain Tumors: Comparison Study with 18FFDG PET and Evaluation of Diagnostic Accuracy. J Nucl Med 2006;47:904-911. Terakawa Y, Tsuyuguchi N, Iwai Y, et al. Diagnostic accuracy of 11C-Methionine PET for differentiation of recurrent brain tumors from radiation necrosis after radiotherapy. J Nucl Med 2008;49(5):694-9. Tang B, Levivier M, Heureux M, et al. 11C-Methionine PET for the diagnosis and management of recurrent pituitary adenomas. Eur J Nucl Med Mol Imaging 2006;33:169-178. Shimizu T, Saito N, Aihara M, et al. Primary Spinal Oligoastrocytoma: A Case Report. Surg Neurol 2004;61:77-81. Wilmshurst JM, Barrington SF, Pritchard D, et al. Positron emission tomography in imaging spinal cord tumors. J Child Neurol 2000;15(7):465-72. Elsinga PH, Hatano K, Ishiwata K. PET tracers for imaging of the dopaminergic system. Curr Med Chem 2006;13(18):2139-53. Berg D. Biomarkers for the early detection of Parkinson’s and Alzheimer’sdisease.Neurodegener Dis 2008;5(3–4):133-6. Broussolle E, Dentresangle C, Landais P, et al. The relation of putamen and caudate nucleus 18F-Dopa uptake to motor and cognitive performances in Parkinson’s disease. J Neurol Sci 1999;166(2):141-51. Koerts J, Leenders KL, Koning M, et al. Striatal dopaminergic activity (FDOPA-PET) associated with cognitive

265

266

17 68.

69.

70.

71.

72.

73.

74.

75.

76.

77.

78.

79.

80.

General imaging modalities: basic principles

items of a depression scale (MADRS) in Parkinson’s disease. Eur J Neurosci 2007;25(10):3132-6. Moore RY, Whone AL, Brooks DJ. Extrastriatal monoamine neuron function in Parkinson’s disease: an 18Fdopa PET study. Neurobiol Dis 2008;29(3):381-90. Drevets WC, Bogers W, Raichle ME. Functional anatomical correlates of antidepressant drug treatment assessed using PET measures of regional glucose metabolism. Eur Neuropsychopharmacol 2002;12(6):527-44. Pardo JV, Sheikh SA, Schwindt GC, et al. Chronic vagus nerve stimulation for treatment-resistant depression decreases resting ventromedial prefrontal glucose metabolism. Neuroimage 2008;42(2):879-89. Lozano AM, Mayberg HS, Giacobbe P, et al. Subcallosal cingulate gyrus deep brain stimulation for treatment of resistant depression. Biol Psychiatry 2008;15:64(6): 461-7. Mayberg HS, Brannan SK, Tekell JL, Silva JA, Mahurin RK, McGinnis S, et al. Regional metabolic effects of fluoxetine in major depression: serial changes and relationship to clinical response. Biol Psychiatry 2000;48:830-843. Mayberg HS, Liotti M, Brannan SK, McGinnis S, Mahurin RK, Jerabek PA, et al. Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry 1999;156:675-682. Liotti M, Mayberg HS, Brannan SK, McGinnis S, Jerabek P, Fox PT. Differential limbic—cortical correlates of sadness and anxiety in healthy subjects: implications for affective disorders. Biol Psychiatry 2000;48:30-42. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C, et al. Deep brain stimulation for treatment-resistant depression. Neuron 2005;45:651-660. Van Laere K, Nuttin B, Gabriels L, et al. Metabolic imaging of anterior capsular stimulation in refractory obsessive-compulsive disorder: a key role for the subgenual anterior cingulated and ventral striatum. J Nucl Med 2006;47(5):740-7. Saxena S, Brody A, Maidment K, et al. Cerebral Glucose Metabolism in Obsessive-Compulsive Hoarding. Am J Psychiatry 2004;161:1038-1048. Schou M, Pike V, Halldin C. Development of radioligands for imaging of brain norepinephrine transporters in vivo with positron emission tomography. Curr Top Med Chem 2007;7(18):1806-16. Cannon DM, Ichise M, Rollis D, et al. Elevated serotonin transporter binding in major depressive disorder assessed using positron emission tomography and (11C)DASB; comparision with bipolar disorder. Biol Psychiatry 2007;62(8):870-7. Meyer JH. Imaging the serotonin transporter during major depressive disorder and antidepressant treatment. J Psychiatry Neurosci 2007;32(2):86-102.

81. Rauch SL, Dougherty DD, Malone D, et al. A functional neuroimaging investigation of deep brain stimulation in patients with obsessive-compulsive disorder. J Neurosurg 2006;104(4):558-65. 82. Yu M. Recent developments of the PET imaging agents for metabotropic glutamate receptor subtype 5. Curr Top Med Chem 2007;7(18):1800-5. 83. Heiss W and Herlolz K. Brain Receptor Imaging. J Nucl Med 2006;47:302-312. 84. Bezrukiy NV, De Salles AAF, Dahlbom M, DeMarco J, Selch M, Smathers J. ‘‘Multimodality Image Fusion for Stereotactic Radiosurgery Planning and Follow-Up’’ Scientific paper exhibit - 87th RSNA annual meeting, Chicago, IL. Radiology 221(P):223, 2001. 85. Maciunas RJ, Galloway RL Jr, Fitzpatrick JM, et al. A universal system for interactive image-directed neurosurgery. Stereotactic Funct Neurosurg 1992;58:108-113. 86. Roberts DW, Strohbehn JW, Hatch JF, et al. A frameless stereotaxic integration of computerized tomographyic imaging and the operating microscope. J Neurosurg 1986;65:545-549. 87. Barnett GH, Kormos DW, Steiner CP, et al. Use of frameless, armless stereotactic wand for brain tumor localization with 20d and 3-D neuroimaging. Neurosurgery 1993;33(4):674-678. 88. Dusick JR, Esposito F, Kelly DF, et al. The extended direct endonasal transsphenoidal approach for nonadenomatous suprasellar tumors. J Neurosurg 2005;102 (5):832-841. 89. Selch MT, Ahn E, Laskari A, et al. Stereotactic radiotherapy for treatment of cavernous sinus meningioma. Int J Radiation Oncology, Biol Phys 2004;59:101-111. 90. Lionberger DR, Weise J, Ho DM, Haddad JL. How does electromagnetic navigation stack up against infrared navigation in minimally invasive total knee arthroplasties? J Arthroplasty 2008;23(4):573-80. 91. De Salles AAF, Pedroso AG, Medin P, Agazaryan N, Solberg T, Cabatan-Awang C, Espinosa DM, Ford J, Selch MT. Novalis Shaped Beam and Intensity Modulated Radiosurgery and Stereotactic Radiotherapy for Spine Lesions. J Neurosurg 2004;101Suppl 3:435-40. 92. De Salles AAF, Melega WP, Lacan G, et al. Radiosurgery with a 3 mm collimator in the subthalamic nucleus and substantia nigra of the vervet monkey. J Neurosurg 2001;95:990-997. 93. Anzai Y, Lufkin R, De Salles AAF, et al. Radiofrequency ablation of brain tumors using MR guidance. Min Invas Ther & Allied Technol 1996;5:232-242. 94. Kim CW, Lee YP, Taylor W, Oygar A, Kim WK. Use of navigation-assisted fluoroscopy to decrease radiation exposure during minimally invasive spine surgery. Spine J 2008;8(4):584-90. 95. Villavicencio AT, Burneikiene S, Bulsara KR, Thramann JJ. Intraoperative three-dimensional fluoroscopy-based computerized tomography guidance for

General imaging modalities: basic principles

percutaneous kyphoplasty. Neurosurg Focus. 2005;15: 18(3):e3. 96. Hamilton AJ, Lulu BA, Fosmire H, Stea B, Cassady JR. Preliminary clinical experience with linear acceleratorbased spinal stereotactic radiosurgery. Neurosurgery 1995;36(2):311-9. 97. Adler JR Jr. Image-guided frameless stereotactic radiosurgery. In: Maciunas RJ editor. Interactive Image-guided neurosurgery. Park Ridge, IL: American Association of Neurological Surgeons; 1993. pp. 81-89. 98. Ryu S, Jin R, Jin JY, Chen Q, Rock J, Anderson J, Movsas B. Pain control by image-guided radiosurgery for solitary spinal metastasis. J Pain Symptom Manage. 2008;35(3):292-8.

17

99. Gorgulho A, De Salles AA, Frighetto L, Behnke E. Incidence of hemorrhage associated with electrophysiological studies performed using macroelectrodes and microelectrodes in functional neurosurgery. J Neurosurgery 2005;102(5):888-96. 100. Gorgulho A, Juillard C, Uslan DZ, Pegues D, Tajik K, Aurasteh P, Behnke E, De Salles AAF. Infection following deep brain stimulator implantation performed in the conventional versus in the MRI operating room. J Neurosurgery, in press. 101. De Salles AAF, Bittar G. Thalamic pain syndrome: anatomical and metabolic correlation. Surg Neurol 1994;41:147-51.

267

24 Image Reconstruction and Fusion B. A. Kall

A wide variety of digital radiological images may be used in stereotactic and functional surgery. These data are generally computed tomography (CT) and variations of magnetic resonance imaging (MRI, MRA, MRV, fMRI etc). Stereotactic data may also be incorporated from other imaging sources like positron emission tomography (PET), single photon emission computed tomography (SPECT) and ultrasound. The variety of applicable imaging sources will continue to grow. Images are created on an image scanning device and transferred to an image-guided system or other off-line computer system for image processing and procedure planning. These systems decode the images, offer a variety of image processing techniques including image reconstruction of two-dimensional slices into a threedimensional volumes, multimodality (CT and MR) or monomodality (T1 MR to T2 MR) image registration and image fusion. Single imaging volumes and/or fused imaging volumes may then registered to the coordinate system of an image-guided device for the surgical procedure or intervention or used postoperatively to confirm an outcome. Registration and Fusion are two image processing techniques that are often used interchangeably, but are not the same. Image registration is a prerequisite for image fusion. Registration is the process of determining a spatial transformation between two coordinate systems. Each imaging scanner produces images in its own three-dimensional coordinate system. Spatial transformations may be calculated between two or more imaging volumes (image registration), between imaging volumes and a stereotactic

#

Springer-Verlag Berlin/Heidelberg 2009

device (stereotactic registration) or between two or more individual imaging volumes and then to a stereotactic device (image registration followed by stereotactic registration). Image fusion is the process of merging or overlaying two or more registered imaging volumes into a hybrid image. The main purpose of nearly all stereotactic planning and intraoperative image-guidance systems is to decode and reconstruct a set of two-dimensional slices into a three-dimensional volume, transform coordinate spaces between one (or more) imaging database(s) and a stereotactic device to precisely aid the stereotactician in the planning and performance of the surgical procedure or treatment. This chapter will review various image reconstruction, registration and fusion techniques utilized in stereotactic and functional surgery.

Introduction to Three-dimensional Radiological Imaging A typical image-guided radiological image dataset is a collection of (contiguous) two-dimensional slices. A medical image scanner defines the location, size and orientation of each slice in its own coordinate system (S). Each slice is typically 512 columns (X) by 512 rows (Y), denoted as 512  512. Some scanners produce slices with a smaller or larger number of rows and columns like 256  256, 128  128 or 1024  1024. Each dot in a slice at a particular row, column intersection is known as a pixel (picture element) and has a two-dimensional size in X and Y measured in millimeters (mm).

336

24

Image reconstruction and fusion

Pixels do not have to be square (same size in X and Y), but usually are collected in that manner for stereotactic procedures. Each pixel is represented internally as a number which represents a gray scale intensity or components of RGB (red, green blue) color so it may be displayed on a computer graphic display. The intensity or color value in some manner is a function of the type of scanner on which the image was produced (e.g., CT intensities are represented in Houndsfield units which are a measure of the attenuation of X-rays). Each image slice (and therefore each pixel) has a location (Z) and thickness in the coordinate system of the scanning device (both usually represented in millimeters). Each component in a medical image is a threedimensional cube known as a voxel (volume element). Each voxel has an X, Y, and Z coordinate and three-dimensional size. The anatomical orientation of a slice is also defined by the scanner (e.g., transverse, sagittal, coronal, oblique). Most image-guided systems and image processing systems for image registration and fusion prefer an imaging series to be scanned as a contiguous set of slices with a homogenous voxel size. In order to facilitate the transfer of images from a scanner to an external device like an image-guided system, the DICOM (Digital Imaging and Communications in Medicine) standard is utilized (http://medical.nema.org). This transfer may be accomplished with tapes, disks or over a network. DICOM adds a header (collection of tags) onto a computer file containing each image which, in addition to containing information like demographics also contains all the relevant information describing how the images were acquired and spatial information to reconstruct them into three-dimensional volumes. An image-guided or image processing system extracts information from the DICOM headers to detect the orientation, coordinate system and voxel dimensions of the imaging series. The individual slices may then be stacked into a three-dimensional volume matrix. In most

circumstances, the volume is reconstructed into homogeneous three-dimensional voxels by interpolation.

Registration Registration is the process of finding a spatial transformation that maps points from one coordinate system (C1) to those in another coordinate system (C2). Image registration is the process of finding a spatial transformation (T) that maps all points in one image/volume to homologous points in another image/volume (> Figure 24-1).

Methods of Registration One image volume is referred to as the reference (or fixed) volume and a second image volume to be registered to the reference volume is generally referred to as the moving (or working) volume when performing image registration. The second volume may be resampled volumetrically to match the reference volume and overlaid or fused with the reference volume and in some instances resliced to match the original slices in the reference volume following registration. . Figure 24-1 Image registration involves determining a spatial transformation (T) that maps points in the coordinate system from image volume 1 (C1) to a matching point in the coordinate system of image volume 2 (C2)

Image reconstruction and fusion

Image registration algorithms are categorized by the type of transformation method employed. Most registration techniques used in stereotactic surgery are rigid (linear) transformations. Rigid registration assumes the images are isotropic in that the original images are not warped, skewed or distorted. A series of rotations and translations are used to calculate the overall mathematical transformation to spatially register two image datasets. Deformable (or elastic) transformations apply additional warping components that may be applied either globally or locally to subsets of the image volumes. Deformable image registration techniques are used more often for intrasubject image registrations as well as to study disease progression (e.g., tumor volume growth) or to register anatomy that moves (heart). Deformable transformations are a useful method to correct geometric distortions in the original imaging data [1]. This chapter will focus primarily on rigid transformation methods while a deformable transformation component may be introduced if the image data is warped or distorted.

Stereotactic Frame Registration The earliest form of multimodality image registration utilized stereotactic frames [2]. The mathematical properties of registering medical images to a stereotactic frame are covered in much detail elsewhere in this textbook. Briefly, a head frame is rigidly attached to a patients head and a localization device with know geometric properties is attached to the head frame when a radiological scan is acquired. The localizer deposits marks in the imaging data. A computer can then transpose every voxel in stereotactically collected image data into the coordinate system of the particular frame using the geometric properties of the localizer. Multiple scans from multiple modalities may be stereotactically collected.

24

In some systems, the headframe can be removed and precisely reapplied to collect data on different days [3]. Once more than one image volume is registered to the coordinate system of the frame, points, volumes and entire scans may be related to each other using the coordinate system of the stereotactic frame [4–7].

Point Matching Registration Point matching registration, also known as iterative closest point registration, is the simplest method of registering two image volumes without a stereotactic frame [8,9]. Neurosurgeons will recognize point matching registration as the manner by which matching points are registered between locations selected on images (anatomical, stickon or screwed in fiducials) and corresponding locations touched on the patient with an imageguided probe in the operating room. A number of N corresponding anatomical points are identified by the user in each imaging set. The point matching algorithm iteratively alters a spatial transformation by applying a stepwise pattern of translations and rotations. The updated transformation is applied to transform coordinate points from the second set and the sum of squares distance between matching points in the two data sets is recalculated. The algorithm iterates (repeats) for new combinations of rotations and translations until the sum of squares measure is minimized usually measured as a root mean square difference (RMS).

Surface/Edge Matching Registration Surface matching is similar in nature to point matching except that the sets of points are extracted from the surfaces or edges of structures in the image data. These surfaces and edges are commonly determined by thresholding segmentation techniques. Surfaces or edges that are

337

338

24

Image reconstruction and fusion

commonly utilized are the skin surface, cortical surface or edges of the ventricular system for cranial procedures or the surface of vertebra for spinal imaging. This method does not require a set of homologous points (> Figure 24-2).

Surface/edge matching may be performed by variations of point matching as well as algorithms generally knows as the ‘‘hat and head’’ method originally developed for registration of CT, MR, and PET Images [10–14]. Surfaces and edges of

. Figure 24-2 Surface-based image registration: (a) determination of surface in Ictal and Interictal SPECT, (b) determination of MRI cortical surface, (c) SPECT hyperperfusion fused to MRI

Image reconstruction and fusion

matching structures are extracted from the imaging data. One set is represented as a cloud of threedimensional points (‘‘hat’’) and the other as a stack of slices (‘‘head’’). A spatial transformation is iteratively calculated by transforming the hat points onto the head surface until the closest fit of the hat on the head is determined. The square of the distances from points on the hat and its corresponding closest point on the head drawn toward the centroid of the head model is the metric that is minimized. This type of surface registration has also been used previously in registering imaging data to an image guided system [14].

Voxel-based Similarity and Mutual Information Registration One drawback to point and surface matching registration is that manual interaction is necessary to identify either matching anatomical points for point matching registration or surfaces/edges using segmentation methods for surface-based registration methods. These can be both time consuming and are often not precisely reproducible. One user may select slightly different matching anatomical points or the threshold parameters utilized may alter the surfaces or edges extracted using segmentation techniques. Voxel-based registration methods involve calculating a spatial transformation by optimizing some particular measure that may be determined directly from the voxel values rather than geometric relationship in point matching and surface matching registration. Woods et al. [15,16] first proposed voxel similarity registration measures based on the premise that the relative grey values of similar tissues in different images would correspond. Voxel similarity measures were further refined by Hill et al. [17] to define a joint histogram approach that shows changes as the alignment converges so that when anatomical structures overlap the histogram shows clusters around

24

the corresponding grey levels of those structures. Dispersions in the clustering decrease as the alignment approaches convergence. Unfortunately these voxel based-techniques assume that the intensities of corresponding anatomy in corresponding image volumes are linearly related, which is not generally true for multimodality registration. Measuresofdispersioninthetwo-dimensional histograms were then proposed. Hill et al. [18] proposed the third order moment and is a measure of the skewness of the distribution while Collignon [19] and Strudeholme [20] proposed entropy, a measure from information theory [21] as a metric of registration. Entropy, in general, is a measure of dispersion of a probability dispersion. Mutual information registration methods, or relative entropy, were then proposed by Viola and Wells [22–25] as well as Collignon et al. [26–28] at about the same time. Briefly, mutual information (MI) is measure of ‘‘the statistical dependence between two random variables or the amount of information that one variable contains about the other’’ [27]. In medical imaging, one random variable is a voxel intensity in one image volume and the second random variable is a voxel intensity in a second image volume. When two image volumes are geometrically aligned, the mutual information of the image intensity values of corresponding voxels is maximized. This image registration method can be performed without human manual interaction and it does not require any linear relationship of the grey level intensities of matching anatomical structures. Mutual information registration is also implemented as an iterative algorithm. An initial transformation is usually calculated to automatically align the centroids of the imaging volumes. Rotations and translations are applied during each iteration (for rigid transformation), the measure of mutual information is recalculated and the iterations continue in a stepwise optimized manner until the mutual information measure is maximized.

339

340

24

Image reconstruction and fusion

Discussion A number of monomodality or multimodality images may be acquired for a stereotactic or functional procedure. These imaging modalities primarily include CT and variations of MR imaging, but may include a variety of other modalities. The number of image sources considered when planning and performing a stereotactic procedure will continue to grow as will the volume of information from each imaging source. Registering mono or multimodality image volumes to correlate points, volumes or entire imaging volumes and in some instances fusing multiple imaging modalities into a hybrid image volume will continue to be a valuable tool for the stereotactician when planning or performing a stereotactic procedure or confirming the outcome. Rigid spatial registration methods are typically used to perform mono and multimodality imaging registration in stereotactic and functional surgery. Deformable transformation parameters may be introduced if geometric distortion or warping of the imaging data is suspected. Stereotactic frame image registration may be the most accurate and failsafe, but cannot be applied retrospectively. Manual registration methods include point matching and surface alignment registration. Point matching registration is the quickest way to register imaging volumes, but is highly dependent on the selection of matching landmarks. Some imaging systems prefer matching points around the area of interest and some work better when the matching points are dispersed around a larger area of the imaging volume. A small change in a threshold value used for extracting surfaces and edges for surface matching registration may produce slightly differing results. More recently developed voxel-based, and specifically mutual information registration techniques, offer an automated method of image volume registration that requires no assumptions about the underlying characteristics of

the imaging intensity information of a specific imaging acquisition. It is imperative that the result of any image registration is validated and verified. All systems that offer image registration and fusion options offer various mechanism for validation and verification and should be used carefully and comprehensively. Registration algorithms may provide a numeric root mean square (RMS) error estimation or graphically depicted ‘‘zones of confidence’’ to estimate how well the algorithm believes the registration aligns. These numeric and graphical confidence methods should be considered secondary to a comprehensive visual review of the registration accuracy over the entire image volume. The moving image volume is usually resampled to match the orientation of the fixed image volume for validation and verification. Typical visual methods for image registration verification and verification include synchronized comparison of internal and external anatomical locations (> Figure 24-3a) or graphical overlay/fusion techniques such as blending (> Figure 24-3b). The two registered volumes may also be validated and verified by displaying one volume in grayscale and one in color and fusing the registered volumes (> Figure 24-3c). Small angular misregistrations may only become apparent by verifying a large number of both internal and external locations throughout the entire image volume (> Figure 24-4). Errors in image registration and fusion may also occur because of underlying problems in the original imaging data. Image registration methods work best with contiguous, thin slice imaging acquisitions. Patient movement during the scan may result in ghost artifacts in the images. Even with high quality control, medical image scanners, and in particular MR scanners may produce imaging containing distortions because of gradient field nonlinearities [29] that may acceptable for diagnostic purposes, but not for quantitative purposes like image registration and

Image reconstruction and fusion

24

. Figure 24-3 Validation and verification techniques: (a) reviewing corresponding points, (b) blending of CT with stereotactic frame and MR frameless, (c) fusing one volume in grayscale (MRI) and one in color (SPECT)

stereotactic surgery. Image registration methods used in stereotactic and functional surgery generally assume that the images are not warped, skewed or distorted.

A routine diagnostic scan performed at a typical institution may not be a good candidate for an image registration because of the relative thickness of each image. Radiological technicians

341

342

24

Image reconstruction and fusion

. Figure 24-4 Small angular misregistration apparent by comparing matching points on CT and MRI

may also not follow appropriately prescribed imaging protocols and by the time the surgeon may want to do an image registration, it may be too late to repeat the imaging study over again. Automated methods of image registration may occasionally not converge on the correct result because the algorithm was not optimized correctly or because the orientation the two original image volumes are too far apart from one another (e.g., neck flexion significantly different between two clinical imaging volumes which is analogous to a straight CT gantry tilt in one image volume and 10–20 gantry tilt in another). Image reconstruction, registration and fusion techniques perform best with high quality images as inputs.

Summary A variety of images from multiple sources may be considered by the stereotactic and functional surgeon for planning a procedure or confirming results. Images from monomodality or multimodalities may be spatially registered and in some instances fused to provide useful information to improve the ability for a positive outcome. Comprehensive verification and validation of manually

or automatically registered or fused volumes is a mandatory step in performing these techniques. When used appropriately, image reconstruction, registration and fusion techniques may be a powerful tool for the stereotactic and functional surgeon.

References 1. Archip N, Clatz O, Whalen S, DiMaio SP, Black PM, Jolesz FA, Golby A, Warfield SK. Compensation of geometric distortion effects on intraoperative magnetic resonance imaging for enhanced visualization. Oper Neurosurg 2008;62(3):209-16. 2. Goerss S, Kelly PJ, Kall B, Alker GJ, Jr. A computed tomographic stereotactic adaptation system. Neurosurgery 1982;10:375-9. 3. KellyPJ, Earnest R, IV, Kall BA, Goerss SJ, Scheithauer B. Surgical options for patients with deep-seated brain tumors: computer-assisted stereotactic biopsy. Mayo Clin Proc. 1985;60:223-9. 4. Kall BA, Kelly PJ, Goerss SJ, Earnest, F, IV. Crossregistration of points and lesion volumes from MR and CT. In: Proceedings of the seventh annual meeting of frontiers of engineering and computing in health care, Chicago; 1985, p. 692–5. 5. Kelly PJ, Kall B, Goerss S, Alker GJ, Jr. A method of CT-based stereotactic biopsy with arteriographic control. Neurosurgery 1984;14:172-7. 6. Kelly PJ, Kall BA, Goerss S. Computer-assisted stereotactic biopsy utilizing CT and digitized arteriographic data. Acta Neurochirurgica 1984; Suppl 33:233–5.

Image reconstruction and fusion

7. Kall, BA, Kelly PJ, Goerss SJ. Comprehensive Computerassisted data collection, treatment planning and interactive surgery. Proc SPIE Med Imaging 1987;767:509-14. 8. Besl PL, McKay ND. A method for registration of 3D shapes. IEEE Trans Pattern Anal Mach Intell 1992;14 (2):239-56. 9. Zhang ZY. Iterative point matching for registration of free-form curves and surfaces. Int J Comput Vis 1994;13(2):119-52. 10. Pelizzari CA, Chen GTY. Registration of multiple diagnostic imaging scans using surface fitting. In: The use of computers in radiation therapy. North-Holland: Elsevier; 1987, p. 437-40. 11. Pelizzari CA, Chen GTY, Spelbring DR, Weichselbaum RR, Chen CT. Accurate three-dimensional registration of CT, PET and MRI images of the brain. J Comput Assist Tomogr 1989;13:1, 20-26. 12. Pelizzari CA, Levin DN, Chen GTY, Chen CT. Image registration based on anatomical surface matching. In: Interactive image-guided neurosurgery. American Association of Neurological Surgeons, New York: Theime; 1993. p. 47-62. 13. Levin DL, Pelizzari CA, Chen GTY, Chen CT, Cooper MD. Retrospective geometric correlation of MR, CT and Pet images. Radiology 1988;169:817-23. 14. Kall BA. Computerized visualization techniques in stereotactic neurosurgery. In: Textbook of stereotactic and functional neurosurgery. New York: McGraw Hill; 1998. p. 351-5. 15. Woods. RP, Cherry SR, Mazziotta JC. Rapid automated algorithm for aligning and reslicing PET images. J Comput Assist Tomogr 1992;16(4):620-33. 16. Woods RP, Mazziotta JC, Cherry SR. MRI-PET registration with automated algorithm, J Comput Assist Tomogr 1993;17(4):536-46. 17. Hill DLG, Hawkes NA, Harrison NA, Ruff CF. A strategy for automated multimodality image registration incorporating anatomical knowledge and imager characteristics. In: Proceedings of the 13th international conference on information processing in medical imaging. LNCS, vol. 687, Berlin: Springer; 1993. p. 182-96. 18. Hill DLG, Studholme C, Hawkes DJ. Voxel similarity measures for automated image registration, visualization in biomedical computing. Proc SPIE 1994;2359:205-16.

24

19. Collignon A, Vandermeulen D, Suetens P, Marchial G. 3D multimodality medical image registration using feature space clustering. In: Proceedings of the first international conference on computer vision, virtual reality and robotics in medicine. LNCS, vol. 905, Berlin: Springer; 1995. p. 195-204. 20. Studholme S, Hill DLG, Hawkes DJ. Multiresolution voxel similarity measures for MR-PET registration. In: Information processing in medical imaging. Dordrecht: Kluwer; 1995. p. 287-98. 21. Cover TM, Thomas JA. Elements of information theory. New York: Wiley; 1991. 22. Wells WM, III, Viola P, Kikinis R. Multi-modal volume registration by maximization of mutual information. In: Medical robotics and computer assisted surgery. New York: Wiley; 1995. p. 55-62. 23. Viola P, Wells WM, III. Alignment by maximization of mutual information. In: Proceedings of the fifth international conference on computer vision (ICCV 95), Boston, MA. IEEE Computer Society Press; 1995. p. 16-23. 24. Viola P. Alignment by maximization of mutual information. Ph.D. Thesis, Massachusetts Institute of Technology, Boston, MA; 1995. 25. Wells WM, Viola P, Atsumi H, Nakajima S, Kikinis R. Multi-modal volume registration by maximization of mutual information. Med Image Anal 1996;1(1):35-51. 26. Collignon A. Multi-modality medical image registration by maximization of mutual information. Ph.D. Thesis, Catholic University of Leuven, Leuven, Belgium; 1998. 27. Collignon A, Maes F, Delaere D, Vandermeulen D, Suetens P, Marchial D. Automated multimodality image registration based on information theory. In: Information processing in medical imaging. Dordecht: Kluwer; 1995. p. 263-74. 28. Maes F, Collignon A, Vandermuelen D, Marchal G, Suetens P. Multimodality image registration by maximization of mutual information, IEEE Trans Med Imaging 1997;16(2):187-98. 29. Wang D, Strungell W, Cowin G, Doddrell DM, Slaughter R. Geometric distortion in clinical MRI systems: part I: evaluation using a 3D phantom. Magn Reson Imaging 2004;22(9):1211-21.

343

23 Neurophysiologic Mapping for Glioma Surgery: Preservation of Functional Areas R. M. Richardson . M. S. Berger

The resection of tumors located within or adjacent to eloquent cortical regions is often necessary to alleviate focal neurological deficits secondary to mass effect and increased intracranial pressure. In addition, there is growing evidence that greater extent of tumor resection correlates with increased time to tumor progression and overall survival for glioma patients [1,2–4]. The surgical aim is to achieve maximal tumor removal without producing permanent morbidity. Neurophysiological mapping of functional areas is critical for minimizing the morbidity associated with removing abnormal tissue from eloquent cortex. Here we present techniques for intraoperative cortical and subcortical stimulation mapping to maximize safe removal of tumors located in motor and language cortex. Cortical stimulation techniques have been adapted from the pioneering methods of Penfield and Boldrey [5], while localization of subcortical motor and sensory tracts was first described by Berger et al. [6].

Asleep Craniotomy with Motor Function Mapping

pathways, it is important to perform both cortical and subcortical stimulation mapping. Regardless of the degree of tumor infiltration, swelling, apparent necrosis, and gross distortion by the tumor mass, functional cortex and subcortical white matter may be located within the tumor itself or the adjacent infiltrated brain [7]. When using stimulation mapping methods to identify subcortical pathways, the surgeon is able to achieve an acceptable risk of permanent motor deficits in patients with gliomas that are within or adjacent to motor tracts.

Preoperative Neurological Evaluation Although motor mapping will often not be useful in patients with severe hemiparesis, if antigravity movement is present preoperatively it is usually possible to stimulate both cortical and subcortical motor pathways intraoperatively. In children younger than 6 years of age, who may have cortical electrical inexcitability, somatosensory evoked potentials must be available and used to identify the central sulcus via phase reversal.

Indications Preoperative Functional Imaging Hemispheric tumors located within or adjacent to rolandic cortex, supplementary motor area (SMA), corona radiata, internal capsule and uncinate fasciculus constitute the major indications for intraoperative motor function mapping. Due to the risk of damaging descending motor #

Springer-Verlag Berlin/Heidelberg 2009

A volumetric MRI scan is obtained preoperatively for use with an intraoperative navigational system. The relation of the tumor to primary motor cortex is assessed by identifying the central or Rolandic sulcus on the rostral cuts of the axial T2-weighted

326

23

Neurophysiologic mapping for glioma surgery: preservation of functional areas

MRI scan. This landmark is always present, regardless of mass effect, and is a reliable marker for the motor strip located within the gyrus directly anterior to the sulcus. The motor cortex can be found on midsagittal cuts by following the cingulate sulcus posteriorly and superiorly to its termination, at which point the motor cortex is directly anterior to this sulcus. On far lateral images, the inferior to mid portion of the motor cortex is localized to a region bisected by a perpendicular line drawn from the posterior corner of the insular triangle. Each of these MRI landmarks is useful for determining the proximity of the lesion to the motor cortex preoperatively. Preoperative functional imaging of primary motor cortex is achieved by magnetic source imaging (MSI), in which the source localization of functional cortical areas by magnetoencephalography (MEG) is coregistered with an anatomic MRI scan [8,9]. MEG is used to detect the magnetic field associated with neuronal activity itself, rather than relying on an indirect correlate such as the hemodynamic response upon which fMRI is based. MEG is generated by dipole currents associated with dendritic excitatory and inhibitory postsynaptic potentials, which produce frequency specific oscillations whose rhythms change upon brain activation. In this way, the somatosensory cortex and motor cortex are reliably localized preoperatively (> Figure 23-1). Resecting brain tumors involves the risk of damaging the descending subcortical motor pathways. Diffusion tensor image (DTI) fiber tracking is a noninvasive MRI technique that can delineate the subcortical course of the motor pathway by modeling three-dimensional local water diffusion along axonal membranes. DTI is used to visualize descending motor pathways starting from a functional cortical site and extending through the corona radiata, posterior limb of the internal capsule and cerebral peduncle [10] (> Figure 23-2). Fiber tracts delineated using DTI can be used to identify the motor tract in deep white matter and define a safety margin around

. Figure 23-1 Magnetic source imaging (MSI) shows the primary motor cortex involving the right second digit. The white tract mesial to the motor peak depicts the subcortical pathway subserving the motor cortex

. Figure 23-2 A diffusion tensor image (DTI) shows the subcortical motor pathway within the cerebral peduncle and upper pons (corticospinal tract) in relationship to a cystic pilocytic tumor involving the upper brain stem. The DTI tract is depicted in white

the tract during tumor resection, a method that has been validated using intraoperative subcortical stimulation mapping of the motor tract and magnetic source imaging [11]. DTI tractography, however, may be limited by tract termination or deviation in regions of peritumoral vasogenic edema and therefore should be used in combination with intraoperative stimulation mapping.

Neurophysiologic mapping for glioma surgery: preservation of functional areas

Surgical Technique After the dura is opened, and the contralateral arm, leg, and face are uncovered to observe for movement, stimulation mapping begins with identification of the motor cortex. A bipolar electrode (5 mm spacing, 60 Hz, 1ms phase duration) is placed on the surface of the brain for 2–3 sec with a current amplitude between 2 and 16 mA. The motor strip is stimulated in the asleep patient with a starting current of 4 mA and increased in 2 mA increments until a motor response is visually identified. A current above 16 mA has never been necessary to evoke sensory or motor responses and should be avoided [12]. The current is reduced to 2 mA when stimulating the awake patient and is raised in 1 mA increments for eliciting responses from both the motor and sensory cortex. At this point, cold Ringer’s lactate solution should be available for immediate irrigation of the stimulated cortex should a focal motor seizure develop. This will abruptly stop the seizure activity originating from the irritated cortex, without using short-acting barbiturates. Multichannel electromyography recording may be used for greater sensitivity in detecting muscle movements, allowing the use of a lower stimulation current and decreasing the risk of stimulation-induced seizure activity. Stimulated brain sites are marked with sterile numbered tickets (> Figures 23-3a and b). First, the inferior aspect of the rolandic cortex is identified by eliciting responses in the face and hand. For leg motor cortex, a strip electrode may be inserted along the falx and stimulated using the same current applied to the lateral cortical surface to evoke leg motor movements. This maneuver is safe because of a lack of bridging veins between the falx and the leg motor cortex. Similarly, a subdural strip electrode may be used to locate the motor strip when the craniotomy is near but not overlying this cortex. Once the motor cortex is defined, the resection proceeds with identification of the descending

23

tracts using similar stimulation parameters. Functional white matter axons are depolarized using the same current parameters applied to the cortex (> Figures 23-4a and b). When movements or paresthesias are evoked, the resection should cease because of the close proximity of intact functional pathways (current spread with bipolar stimulation is 2–3 mm from the electrode contacts). Following completion of tumor resection, a final stimulation of previously identified cortical motor sites confirms that underlying functional tracts have been preserved, which is equally valuable in cases where subcortical responses are not obtained. The presence of intact cortical and subcortical motor pathways implies that any surgery-related deficit would likely be transient, with resolution in days to weeks. In the senior author’s experience with surgery for hemispheric gliomas within or adjacent to the rolandic cortex, patients whose subcortical pathways were identified with stimulation mapping were more prone to develop an additional (temporary or permanent) motor deficit than those in whom subcortical pathways could not be identified (27.5% vs. 13.1%) [23]. Although motor deficits that lasted more than 3 months occurred in 7.4% of the patients whose subcortical pathways were identified, compared to 2.1% of those without subcortical responses, very few patients have been left with a dense paresis using this method.

Awake Craniotomy with Language Function Mapping Indications Due to the discrete localization of essential language areas in the individual patient and great variation in their location across the population, an awake craniotomy with cortical stimulation mapping is indicated for any lesion involving the dominant temporal, mid- to posterior frontal, and mid- to anterior parietal lobes. Stimulation

327

328

23

Neurophysiologic mapping for glioma surgery: preservation of functional areas

. Figure 23-3 Intraoperative mapping of the motor cortex involving the hand and shoulder is shown (a). The tumor is seen on the sagittal MRI scan to be located within the supplementary motor area (b)

mapping has shown that multiple discrete areas in perisylvian cortex of the dominant hemisphere as essential for language functions, with separation of areas for different aspects of language, including naming in two languages, different semantic classes, naming compared to reading, and language from verbal memory [12]. Sites where stimulation repeatedly interferes with naming have been localized to focal areas of approximately 1 cm2 in the dominant hemisphere cortex, frequently with one such site in perisylvian inferior frontal cortex and several others in temporoparietal cortex [13]. The exact location of these sites in the language dominant hemisphere varies substantially across the patient

population, particularly in temporoparietal cortex, with random distribution within the temporal lobe and in the inferior posterior frontal and anterior inferior parietal lobes. Additionally, no specific region of the temporal lobe cortex may be found to be essential for language function in many patients (55% in the study referenced above). With regard to bilingual patients, cortical stimulation studies have demonstrated the existence of both shared and distinct languagespecific cortical centers. In one study of 25 bilingual patients, primary and secondary language representations were similar in total cortical extent, but differed in anatomical distribution [14].

Neurophysiologic mapping for glioma surgery: preservation of functional areas

23

. Figure 23-4 Enhanc