Handbook of Pediatric Strabismus and Amblyopia

Handbook of Pediatric Strabismus and Amblyopia Handbook of Pediatric Strabismus and Amblyopia Edited by Kenneth W. Wr...

Author: by Kenneth W. Wright (Editor) | Peter H. Spiegel (Editor) | Lisa Thompson (Editor)

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Handbook of Pediatric Strabismus and Amblyopia

Handbook of Pediatric Strabismus and Amblyopia Edited by

Kenneth W. Wright, MD Director, Wright Foundation for Pediatric Ophthalmology Director, Pediatric Ophthalmology, Cedars-Sinai Medical Center, Clinical Professor of Ophthalmology, University of Southern California—Keck School of Medicine, Los Angeles, California

Peter H. Spiegel, MD Focus On You, Inc., Palm Desert, California Inland Eye Clinic, Murrieta, California Children’s Eye Institute, Upland, California

Lisa S. Thompson, MD Attending Physician, Stroger Hospital of Cook County, Chicago, Illinois

Illustrators Timothy C. Hengst, CMI Susan Gilbert, CMI Faith Cogswell

Kenneth W. Wright, MD Director, Wright Foundation for Pediatric Ophthalmology Director, Pediatric Ophthalmology, Cedars-Sinai Medical Center, Clinical Professor of Ophthalmology, University of Southern California—Keck School of Medicine Los Angeles, CA USA

Peter H. Spiegel, MD Focus On You, Inc. Palm Desert, CA Inland Eye Clinic, Murrieta, CA Children’s Eye Institute Upland, CA USA

Lisa S. Thompson, MD Attending Physician Stroger Hospital of Cook County Chicago, IL USA

Library of Congress Control Number: 2005932932 ISBN 10: 0-387-27924-5 ISBN 13: 978-0387-27924-4

e-ISBN 0-387-27925-4

Printed on acid-free paper. © 2006 Springer Science+Business Media, Inc. Reprinted from Wright and Spiegel: Pediatric Ophthalmology and Strabismus, second edition, 2003 Springer Science+Business Media. All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer Science+Business Media, Inc., 233 Spring Street, New York, NY 10013, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identiﬁed as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights. While the advice and information in this book are believed to be true and accurate at the date of going to press, neither the authors nor the editors nor the publisher can accept any legal responsibility for any errors or omissions that may be made. The publisher makes no warranty, express or implied, with respect to the material contained herein. Printed in the United States of America. 987654321 springer.com

(BS/EB)

Preface

The Handbook of Pediatric Strabismus and Amblyopia is a practical, easy-to-understand resource on the diagnosis and management of both common and the more esoteric forms of strabismus. Emphasis is placed on the understanding of the basis of the strabismus, not rote memorization of strabismus patterns. Concepts regarding sensory adaptations and sensory testing are described in a simple way to elucidate rather than confuse the reader. An in-depth chapter on visual development and the pathophysiology of amblyopia is included. The goal of the Handbook of Pediatric Strabismus and Amblyopia is to make this often confusing subject simple and easy to understand. This book should make an excellent resource for board review. Chapters are reader friendly. They are organized with clear sub-headings that allow the readers to quickly ﬁnd their area of interest. Diagrams and drawings are prevalent throughout the book to help illustrate otherwise difﬁcult or complex concepts. Composite strabismus photographs are included to demonstrate the strabismus as it actually appears in the clinical setting and to help with pattern recognition. These composite strabismus photographs are very useful for board review. Each chapter is fully referenced to provide evidence-based practice guidelines and further in-depth reading. An important use of the handbook is patient and family education. Families are rightfully concerned about the strabismus and they have often been told conﬂicting and confusing information about it. Information, including diagrams and photographs from the handbook, can be shared with the families to clarify their speciﬁc type of strabismus. This important information is often lacking in general texts on ophthalmology. v

vi

preface

I hope you will ﬁnd the Handbook of Strabismus and Amblyopia to be an invaluable adjunct to your practice and for board review. Kenneth W. Wright, MD

Contents

Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Contributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

v ix

1 Pediatric Eye Examination . . . . . . . . . . . . . . . . . . Ann U. Stout

1

2 Anatomy and Physiology of Eye Movements . . . . Kenneth W. Wright

24

3 Binocular Vision and Introduction to Strabismus . . . . . . . . . . . . . . . . . . . . . . . . . . . . Kenneth W. Wright

70

4 Visual Development and Amblyopia . . . . . . . . . . . Kenneth W. Wright

103

5 The Ocular Motor Examination . . . . . . . . . . . . . . Kenneth W. Wright

138

6 Sensory Aspects of Strabismus . . . . . . . . . . . . . . . Kenneth W. Wright

174

7 Esodeviations . . . . . . . . . . . . . . . . . . . . . . . . . . . . Kenneth W. Wright

217

8 Exotropia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Kenneth W. Wright

266

9 Alphabet Patterns and Oblique Muscle Dysfunctions . . . . . . . . . . . . . . . . . . . . . . Kenneth W. Wright

284

vii

viii

contents

10 Complex Strabismus: Restriction, Paresis, Dissociated Strabismus, and Torticollis . . . . . . . . Kenneth W. Wright

323

11 Strabismus Surgery . . . . . . . . . . . . . . . . . . . . . . . . Kenneth W. Wright and Pauline Hong

388

12 Ocular Motility Disorders . . . . . . . . . . . . . . . . . . Mitra Maybodi, Richard W. Hertle, and Brian N. Bachynski

423

13 Optical Pearls and Pitfalls . . . . . . . . . . . . . . . . . . David L. Guyton, Joseph M. Miller, and Constance E. West

520

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

531

Contributors

Brian N. Bachynski, MD David L. Guyton, MD Richard W. Hertle, MD, FACS Pauline Hong, MD Mitra Maybodi, MD Joseph M. Miller, MD Ann U. Stout, MD Constance E. West, MD Kenneth W. Wright, MD

ix

1 Pediatric Eye Examination Ann U. Stout

THE HISTORY AND PHYSICAL EXAMINATION In the nonpediatric eye clinic, the physician often views the presence of a small child in an examining lane with some anxiety, if not dread. Examination of a child is quite different from that of the adult. The history is largely from a source other than the patient, and the examination requires patience and talent. There are several tricks to make the visit go as smoothly and efﬁciently as possible (see the box on the following page).

HISTORY Although ancillary personnel are often relied on to take the history, this is best obtained by the physician who knows how to direct the line of questioning to the most useful information. The old adage that “the patient is always right” is especially true in the case of parents’ observations about their children. Most of the history is obtained from the parents or the referring physician, but any input from the child is equally important. Many children will not complain of blurry vision or diplopia, but should they describe these symptoms one must be very alert to an acute process. This is also an invaluable time to observe the child in an unobtrusive fashion and preliminarily assess head position, eye alignment, and overall appearance. Often this may be the extent of the physical examination that one can obtain; once children realize that attention is focused on them, they may become very uncooperative. The problem precipitating the visit should be stated in the parents’ or child’s own words and then elaborated. Requisite 1

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handbook of pediatric strabismus and amblyopia

questioning for all pediatric eye problems should clarify whether the problem is congenital or acquired and should specify the age of onset in the latter case. If the chief complaint is a visual problem, it is helpful for the parents to specify what the child can or cannot see; that is, does the child respond to lights, faces, toys near or far, very small items? In cases of strabismus, the frequency and stability of the deviation and any associated head posture are important. Precipitating factors may include fatigue, illness, sunlight, and close or distance work. For nystagmus, medications and the past medical history may be pertinent. With cataracts, any history of trauma, medications, or associated medical conditions is important, as well as the family history. Tearing patients need to be questioned about any redness, photophobia, or crusting of the lashes. In ptosis, the stability or variability is important, as is any associated chin elevation or general neuromuscular problems. For difﬁculties in school, it is helpful to determine if the problem is only visual or is related to a particular subject area (reading, spelling, writing, or math) and if there are any stress factors in the child’s extracurricular life. Important aspects of past history include prenatal and perinatal problems, birth weight, gestational age, and mode of delivery. Any medical problems should be elicited, as well as current medication and allergies. Early development should be assessed by asking about speciﬁc developmental milestones, such as rolling over, sitting up, and walking. The Denver Developmental Scale is a good reference for developmental norms.10 Later development can be ascertained by asking about scholastic level and performance. The family history is very important because often the young child does not have enough past history to be useful. The focus should be on the presence of strabismus, poor vision, and neurological problems. In the case of possible genetic disorders, the number and sex of siblings, possible consanguinity, and the number and gestational age of any miscarriages should be documented.

PHYSICAL EXAMINATION Establishing Rapport If you approach the examination with dread, the child will sense your personal tension and become uneasy. Children can be unpredictable, noncommunicative, and uncooperative, which

chapter 1: pediatric eye examination

3

may make the examination both time consuming and frustrating for a busy practitioner. However, if extra time is taken initially to gain the trust of the child, the rest of the exam will go much more easily. This “friendship” is often first established in the waiting room, where toys, appropriate books, and even small furniture should be made available. In a general practice seeing children on a fairly regular basis, at least one exam room should be outfitted to make a child feel relaxed and make the exam go more smoothly. A 20-foot lane is best because of the frequent use of single Allen cards and the need for distance measurements in strabismus. Attention-getting distance targets may include a remote control cartoon movie or a motorized animal. Near targets should have variety and appeal, as one frequently finds that “one toy–one look” is the rule. Approach young children as though you had come to play with and entertain them, and you will receive a lot of useful information in the process. Find out what they like to be called and use their name frequently, but speak softly and keep a respectful physical distance from them until they warm up to you. Also, ﬁnd out from parents their favorite imaginary or cartoon characters and refer to these during your exam. Make a game of the exam; play peek-a-boo with cover testing, swoop near targets around like an airplane to evaluate the range of motility, refer to glasses and lenses used as “magic” or “funny

Useful Items for Pediatric Eye Exams Allen cards (single and linear) Wright ﬁgures (single and linear) Tumbling E (single and linear) Eye patches Interesting distance and near ﬁxation targets Accommodative near targets (ﬁnger puppets, wiggle pictures) Portable slit lamp Papoose board Wire lid speculums (infant and child size) Loose retinoscopy lenses Loose prisms Fusional tests (Worth 4-Dot, Titmus or Randot, Bagolini lenses) 28-diopter lens Handheld tonometer (Perkins or Tonopen) Calipers

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handbook of pediatric strabismus and amblyopia

sunglasses,” make funny sounds to get their attention. Do the noncontact things ﬁrst: cover testing, ﬁxation testing, pupillary and red reﬂex exam. Many small children object to physical contact by a stranger and once they are upset it is usually the end of the exam for the day. Sometimes they will more readily tolerate their parents placing glasses or a patch than a strange doctor. Remember, if you ﬁnd yourself getting frustrated or impatient with a child in one area, stop and go on to some other aspect of the exam. With older children, asking direct questions about their hobbies, school, and family shows an interest in them and often distracts them from the anxiety of the exam. They often appreciate a handshake or pat on the knee. Explain to them what you are doing before you do it and be honest; avoid talking down to them. If they ask, do not tell them the mydriatic drops will not hurt, but explain that they will only sting for a minute, like swimming in a pool with chlorine.

Examination of the Uncooperative Child Sometimes, despite the best efforts, a child simply will not cooperate, and urgency of the problem or the need for further information may require physically restraining or sedating the child. A papoose board can be used to control a child up to around 5 years of age, depending on their size and strength. A lid speculum can then be used with a topical anesthetic to force the eyes open, although Bell’s phenomenon of the eyes often makes a thorough examination difficult, and crying can affect intraocular pressure measurements.

SEDATION For the child in whom relaxation is important, or when physical restraint seems too psychologically traumatic, as in older children, sedation should be used. The common modes of outpatient sedation include chloral hydrate (oral or suppository), Propofol infusion, or a combination injection of Demerol, Phenergan, and Thorazine (DPT). The ﬁrst has the advantage of good sedation with a low level of respiratory depression and no effect on intraocular pressure (IOP). The latter two have analgesic as well as sedative properties, which may be useful in painful procedures, but there is slightly more respiratory depression and Propofol will lower IOP.24,37

chapter 1: pediatric eye examination

5

Although chloral hydrate is often not effective if the children are more than 2.5 years old, Propofol and DPT can be used in older children. Whenever sedatives are given, the child’s vital signs including pulse oximetry must be monitored until awake, ventilatory equipment must be available, and appropriately trained personnel should be in attendance. Any sedative may have a greater effect in children with underlying neurological abnormalities.

CHLORAL HYDRATE The minimal effective dose of chloral hydrate is 50 mg/kg, but often 80 to 100 mg/kg is needed if manipulation of the eyes is anticipated or if prolonged sedation is needed for electrophysiological testing.9,45,46 Half the initial dose can be repeated up to a maximum of 3 g if the child is not sedated in 30 min.22 Any sedative is best given on an empty stomach (4 h since eating) to increase absorption and decrease the risk of aspiration.

DPT DPT is given in a dose of 2 : 1 : 1 mg/kg, not to exceed 50 : 25 : 25. Because of the better analgesic effects, this is probably a better choice for painful procedures (laceration repairs, chalazion excisions, cryotherapy). Potential complications include respiratory depression, apnea, dystonic reactions, hypotension, seizures, and cardiac arrest.37 This mode of sedation should only be used when the child is under the supervision of a physician with appropriate training to manage complications, as in the emergency room.

EXAMINATION UNDER ANESTHESIA If it is impractical to sedate the child in the ofﬁce, or if surgery is anticipated based on the exam ﬁndings, than examination under anesthesia should be arranged in the operating room. Modern anesthetic practices make general anesthesia a very safe procedure, even when done repeatedly. A disadvantage of general anesthesia is the purported intraocular pressure-lowering effects of inhalational anesthetics. Pressures taken under inhalational anesthetics have been lower than those measured in awake children, but this is probably a result of increased overall relaxation.13 Propofol has a similar effect on IOP.25 The pressure may actually increase several points after intubation.40 Use of laryngeal mask airways may eliminate this transient pressure rise.43 It is probably best to record the pressure both before and after intubation.

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handbook of pediatric strabismus and amblyopia

External Examination The child’s overall appearance and level of alertness can be judged during the history taking. Head posture may also be noted then, as well as gross ocular alignment. The history or appearance may warrant more detailed examination of overall neuromuscular tone, cranial nerves, head circumference, extremities, or skin. The head may be assessed for symmetry, preauricular skin tags, ear position, and shape. The orbits should be appraised for ptosis, abnormalities in ﬁssure size or shape, and orbital depth. Many of these ﬁndings do not require a systematic search but rather an overall heightened awareness of what is normal versus abnormal. The general assessment of a dysmorphic child should push the physician to more precisely deﬁne what abnormalities lead to that impression.

Visual Acuity Assessment: Preverbal To judge vision in the preverbal child, one must rely on the smallest age-appropriate target that will hold attention and on the difference, if any, between the two eyes. An appropriate target for a 1-year-old child may be a small ﬁnger puppet; but a 1-month-old may ﬁxate only on a human face and do that rather unsteadily. Infants are unable to pursue targets smoothly until 6 to 8 weeks of age but instead will track using hypometric saccades.5 Targets with ﬁne detail that require accommodation and focused attention are best for children over age 1, for even though accommodation is appropriate to target distance by age 3 to 4 months, the macula is still immature even at the age of 15 months.6 Children who have developed a pincer grasp can be asked to pick up small particles from the palm of your hand. Often cake sprinkles are useful because they are edible and such a target often ends up in the mouth.

FIXATION There are two types of ﬁxation testing: monocular and binocular. In monocular ﬁxation testing one assesses whether the patient ﬁxes with the fovea (centrally) and the quality of ﬁxation. Each eye should be occluded in turn and the smallest possible target that elicits a ﬁxation response should be used. Monocular ﬁxation should be assessed for three separate factors: quality and accuracy (good, fair, poor), location (central versus eccentric), and duration (maintained versus sporadic). Clinically, abbreviations

chapter 1: pediatric eye examination

7

are often used to describe ﬁxation including GCM for good, central, and maintained, CSM for central, steady, and maintained, or FF for ﬁx and follow. Eccentric ﬁxation is an important sign as this shows that the patient is not ﬁxing with the fovea and vision is in the range of 20/200 or worse. It is important to remember, when testing monocular ﬁxation, that the ﬁxation target should be slowly moved through the visual ﬁeld to assess the quality of ﬁxation. The target size and distance should be estimated and documented in the chart. It is important to be aware of the normal timetable for visual maturation, although this may vary widely with individuals. The newborn has only sporadic saccadic eye movements with very poor ﬁx and follow; by 6 weeks, most infants will show some smooth pursuit and central ﬁxation, and by 8 weeks the vast majority of infants will have central ﬁxation with accurate smooth pursuit and easily demonstrate optokinetic drum responses.6 Smooth pursuit is asymmetrical until age 6 months of age, with monocular temporal to nasal pursuit being better than nasal to temporal pursuit. Tables 1-1 and 1-2 outline normal visual development. One should remember that there is a subgroup of patients who are otherwise normal yet show delayed visual maturation. However, even this group of patients should show improvement of visual function and should have central ﬁx and follow by at least 6 months, with occasional delays up to 12 months of age. Binocular ﬁxation preference compares the vision of one eye to the other. This test presumes that strong ﬁxation preference in patients with strabismus indicates organic visual loss or

TABLE 1-1. Normal Visual Development. Pupillary light reaction present: 30 weeks gestation Blink response to visual threat: 2–5 months Fixation well developed: 2 months Smooth pursuit well developed: 6–8 weeks Saccades well developed (not hypometric): 1–3 months Optokinetic nystagmus (OKN) 1. Present at birth but with restricted slow-phase velocity. 2. Temporal to nasal monocular response better than nasal to temporal until 2–4 months. Accommodation appropriate to target: 4 months Stereopsis well developed: 3–7 months Contrast sensitivity function well developed: 7 months Ocular alignment stabilized: 1 month Foveal maturation complete: 4 months Optic nerve myelination complete: 7 months to 2 years

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handbook of pediatric strabismus and amblyopia

TABLE 1-2. Age-Related Visual Acuity Estimates by Test Method. Technique

Birth

2 months

4 months

6 months

1 year

Age for 20/20 (months)

OKN FPL VEP

20/400 20/400 20/800

20/400 20/400 20/150

20/200 20/200 20/600

20/100 20/150 20/400

20/60 20/50 20/20

20–30 18–24 6–12

OKN, optokinetic nystagmus; FPL, forced-choice preferential looking; VEP, visual evoked potential.

amblyopia in the nonpreferred eye.12,48 Binocular testing has an advantage over monocular testing, because vision can be very poor (20/100 to 20/200) and the patient will still show essentially normal monocular ﬁxation. Binocular ﬁxation preference testing, however, will identify even mild amblyopia (two lines of Snellen acuity difference).44,47 It is important to assess monocular ﬁxation before ﬁxation preference testing to rule out the possibility of bilateral symmetrical visual loss in preverbal children. Fixation preference testing is very accurate for diagnosing amblyopia in children with large-angle strabismus.48 In patients with straight eyes or microtropias, binocular ﬁxation preference testing can be done using the vertical prism test or induced tropia test.47 In patients with straight eyes, one does not know which eye is ﬁxing; therefore, it is impossible to determine ﬁxation preference. The vertical prism test induces a vertical deviation and therefore allows assessment of ﬁxation preference. In patients with small-angle strabismus (less than 10–15 prism diopters), the induced vertical tropia dissociates peripheral fusion and eliminates any facultative suppression scotoma associated with the patient’s baseline ocular alignment. In turn, this eliminates the problem of overdiagnosis of amblyopia, previously described by Zipf.48 Fixation preference testing is a quick and accurate way of diagnosing amblyopia in clinical conditions such as anisometropic amblyopia, unilateral ptosis, postoperative congenital esotropia, and other conditions that could cause unilateral amblyopia.

OPTOKINETIC NYSTAGMUS Children with poor ﬁxation to any targets as a result of either poor vision or central nervous system problems can be evaluated for the presence of optokinetic nystagmus (OKN) so long as they are able to generate saccades. Optokinetic nystagmus is an involuntary pursuit response to moving stripes ﬁlling up

chapter 1: pediatric eye examination

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most of the visual ﬁeld, so a response may be seen in infants who are merely uninterested in other targets. Response to a standard OKN drum implies vision of ﬁnger counting at 3 to 5 feet.16,17 One can also assess the damping of the induced vestibulo-ocular reﬂex. By spinning the child around, either in your arms or on a swivel chair, a vestibular nystagmus will be induced, despite the level of vision. If there is visual input once the spinning is stopped, the nystagmus should damp in 30 to 60 s due to the ﬁxation reﬂex.

OTHER TESTS Many ingenious tests have been devised to try to better correlate the vision to a linear acuity and detect amblyopia. The most popular are forced-choice preferential looking (FPL) and pattern visual evoked potentials (PVEP). The preferential looking test using Teller acuity cards assesses grating acuity by presenting the child with high-contrast gratings of various spatial frequencies along with a paired blank card. Infants will naturally prefer to look at patterns if they can be seen, and the examiner assesses whether the child ﬁxates on the pattern or not.36 This test reliably measures grating acuity, but it may take 20 to 30 min to perform and may be difﬁcult to perform monocularly in children younger than 2 years old33 (Fig. 1-1). Although useful in the assessment of anisometropic or deprivation amblyopia, this test

FIGURE 1-1. Teller acuity preferential looking apparatus.

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handbook of pediatric strabismus and amblyopia

FIGURE 1-2. Two Polaroid photogrpahs from MTI PhotoScreener, taken by a rotating ﬂash. The white crescent in the pupils denotes a refractive error. The size and location of the crescent in each photo indicate the type and example of the problem. Findings: hyperopia, 2.00 D; astigmatism, 1.00 D. The displaced corneal light reﬂex demonstrates esotropia.

may underestimate strabismic amblyopia or decreased acuity secondary to macular disease, in which grating acuity may be much less affected than vernier and Snellen acuity. Therefore, although a detected difference conﬁrms amblyopia, a normal test result does not rule out amblyopia.26 Fixation preference testing is more reliable in detecting strabismic amblyopia. PVEP measures the summed occipital cortical response to a pattern stimulus (Fig. 1-2). This method reﬂects the activity from the central retina and is therefore a good assessment of macular function.32 The resulting cortical potential can be evaluated by a trained electrophysiologist and Snellen acuity can be roughly estimated. The important parameters of the PVEP waveform are the amplitude and the latency of the spikes. The ﬁrst major large positive deﬂection is the P1 spike, with a normal latency of 100 ms. Amblyopia diminishes the amplitude, as do uncorrected refractive error or organic problems. The difﬁculty in the test lies in the need for specially trained personnel to administer and interpret the test and the frequent need for seda-

chapter 1: pediatric eye examination

11

tion to get good results. Although the test can be administered while the child is awake, poor ﬁxation may give artiﬁcially low results. In the sedated child (chloral hydrate), cycloplegia and appropriate refractive correction are necessary because retinal blur also affects test results.45,46 Despite these drawbacks, the test is often useful to monitor the progress of amblyopia therapy and to diagnose amblyopia in preverbal children.

Visual Acuity Assessment: Verbal OPTOTYPE Older children who are able to identify character shapes can be assessed with Allen cards, Wright ﬁgures, or Lea symbols.18 Often, a child who is not quite verbal, or is too shy to talk, can be asked to match a sheet of pictured ﬁgures to the displayed cards. The single cards are most useful in the beginning, because often the child does not attend well to distance targets such as projected ﬁgures. The child can also take a photocopy of the cards home to practice as a game with parents. It is best to start close to the child and work backward. In young children, the endpoint is more often demonstrated by a loss of attention than by an incorrect response. The disadvantage of single cards is that they cannot detect the crowding response that is so often seen in amblyopia. A child may test equally on single optotypes but show a marked discrepancy with linear optotypes.34 Once equal acuity is obtained on single cards, it is important to move to linear testing to conﬁrm the ﬁndings. Both single and linear ﬁgures test only to the level of 20/30, which is adequate for children under the age of 3 years. The next step in preliterate testing is use of the tumbling E, Wright ﬁgures, or HOTV.18 With the “E game,” the child is asked to point his ﬁngers in the direction of the “legs on the table.” Often, vertical orientations are more readily confused by children than horizontal directions, and this should be taken into account when determining the endpoint.39 The HOTV letters can be easily identiﬁed even if the full alphabet is not known. Again, single cards or linear projection can be used, the latter being best for amblyopia. These tests go to the 20/20 level and are slightly more challenging than picture cards. Once the child is literate, traditional Snellen letters can be used. For most children, this occurs around age 5 to 6, but do not confuse knowing the alphabet with being able to distinguish

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handbook of pediatric strabismus and amblyopia

random letters. If in doubt about the reliability of letter testing, return to an easier test.

Visual Fields As soon as a child is able to ﬁx steadily on a target, a rough estimate of visual ﬁelds can be obtained. Even if the child will not tolerate a patch, binocular ﬁelds can be checked for homonymous or bitemporal defects. Infants with good ﬁxation will usually move to an interesting peripheral target once it comes into view as a result of the ﬁxation reﬂex. The examiner captures the attention with a central target and then slowly brings in a peripheral target, watching for the ﬁrst jump to the peripheral target. In this manner all four quadrants of the peripheral ﬁeld can be tested. Patients with posterior optic pathway lesions that respect the vertical meridian will often ignore a peripherally advancing target until it crosses the midline and then suddenly move and pursue it. A slightly older child of 3 or 4 years may be able to respond accurately to ﬁnger counting by making a game of copying the examiner’s actions. Formal visual ﬁeld testing such as Goldmann perimetry can sometimes be performed in preschool children. It is important to have a good idea of the suspected ﬁeld loss and concentrate on these areas ﬁrst. Usually the largest brightest target (V4e) is best, but smaller targets should be used if the child is capable of cooperating. Automated ﬁelds require prolonged concentration and steady ﬁxation and are usually not reliable in children less than 9 to 10 years old. Some newer user-friendly programs are being developed that shorten testing time enough to make them more applicable for children (Welch Allyn; frequency doubling technology or FDT). The tangent screen is also not useful until reliable verbal responses can be made because it is difﬁcult to monitor ﬁxation.

Assessment of Color Vision in Children Although color vision testing is not often done in children, it helps in the diagnosis of decreased acuity of uncertain etiology and monitors progression in cases of macular degenerations or progressive optic neuropathies. Children on retinal toxic drugs also need to be evaluated. Congenital red-green color defects are often detected ﬁrst by the pediatric ophthalmologist as an incidental ﬁnding. Screening questions are often useful in detecting

chapter 1: pediatric eye examination

13

these cases, which occur in 8% to 10% of the male population. The child may confuse green with brown crayons and purple with blue crayons; he may confuse yellow and red trafﬁc lights or green and red lines on a paper. Often he will have no trouble accurately naming colors of large objects but will mistake smaller colored objects subtending less than 2°.5 The easiest way to screen for color vision defects is with color plates. There are two popular types of plates, which are each useful in speciﬁc situations. The Ishihara pseudoisochromatic color plates work on the principle of color confusion, which is common with dichromats and anomalous trichromats. These plates are extremely sensitive for red-green defects, which are usually congenital. Most acquired color defects show some loss in the blue-yellow range, and the Ishihara plates will miss these patients unless the loss has extended into the red-green range. The advantage of these plates is that they come in an illiterate form with geometric shapes that can be traced with a ﬁnger. This design is useful for children who do not know numbers but still requires the comprehension and ﬁne motor skills of a 3- to 4-year-old. The Richmond pseudoisochromatic plates, formerly called American Optical Hardy-Rand-Rittler (AO-HRR) plates, work on color saturation and can detect both red-green and blue-yellow defects, making them more useful in acquired defects; unfortunately, these do not come in an illiterate format. Both tests use many two-digit numbers, which can intimidate young children, and often their responses are better if they are asked to name each digit separately. Another good test for children is the City University Color Vision Test (TCU test); this uses the colors in the Farnsworth D-15 in a book format, so that manipulation of the color discs is not necessary. Unfortunately, it is not the best test for screening, as 20% of color defectives will pass the test. In general, optic nerve disease is more likely to affect red-green perceptions, whereas retinal disease affects blue-yellow discrimination, although there are many exceptions to this rule.16,17

Assessment of Contrast Sensitivity Contrast sensitivity represents the minimal amount of contrast required to resolve various-sized objects from the background. As such, it is perhaps a more sensitive test of visual function than Snellen acuity, which only assesses high-contrast resolution. The contrast sensitivity threshold is the minimal amount

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handbook of pediatric strabismus and amblyopia

of contrast required to detect sinusoidal gratings of different spatial frequencies. The contrast sensitivity function (CSF) is the curve obtained by plotting contrast sensitivity against spatial frequency. The peak of the curve is usually at three to four cycles per degree, although the maximal contrast sensitivity for each spatial frequency increases with age to stabilize in adolescence. Contrast sensitivity may show decrements in many disease processes despite a normal Snellen acuity, including cerebral lesions and multiple sclerosis.4 Amblyopes demonstrate a reduction in the CSF curve that may occur only at the peak (highfrequency loss) or throughout the curve (high- and low-frequency loss).20 This difference persists after Snellen acuity returns to normal and may be useful in detecting a continued need for amblyopia therapy.31A Occlusion therapy for amblyopia has also been shown to reduce contrast sensitivity in the dominant eye, even without decreased acuity, a type of mild occlusion amblyopia.24 Although testing previously required fairly complex equipment and was not suitable for young children, contrast sensitivity function can now be reliably measured on children over 4 years using the Vistech wall chart. The chart presents eight levels of contrast sensitivity (horizontal axis) for each of ﬁve levels of spatial frequency (vertical axis). The gratings are oriented in one of three directions, 15, 0, or 15, and the child imitates grating orientation with his hand as in the “E game.” The minimum contrast detectable at each spatial frequency is recorded and used to plot a contrast sensitivity function curve.

Red Reﬂex Evaluation of the red reﬂex is often forgone in adults because of the better sensitivity of other available tests; that is, visual acuity and high-power biomicroscopy of the anterior segment, lens and vitreous. In children, these tests may not be applicable for reasons of youth or lack of cooperation. Evaluation of and especially binocular comparison of the red reﬂex are invaluable in assessing media opacities or refractive aberrancies. The red reﬂex is best tested by staying far enough away from the child to illuminate both pupils with the same direct ophthalmoscope beam and comparing the quality and intensity of the reﬂexes between the two eyes. The exam should be done in dim illumination, to encourage pupil dilatation, and with the child’s attention focused in the distance, to avoid a near response. If the direct ophthalmoscope beam is too strong, the pupils will con-

chapter 1: pediatric eye examination

15

strict and the child will react to the brightness by blinking or turning away. It is important to assess the reﬂex both before and after dilation, especially if there is a visually signiﬁcant opacity, to see how much of the undilated pupillary space is obscured. Dimming of the red reﬂex is also an important sign in early endophthalmitis after cataract or strabismus surgery. Bruckner described a useful test for strabismus using the red reﬂex from the direct ophthalmoscope. In the presence of strabismus, the red reﬂex will be brighter and the pupil will appear slightly larger in the deviated eye as the patient ﬁxates on the light. This test can detect deviations as small as three prism diopters and is especially useful in evaluating postoperative alignment.38 The test can be carried a step further to evaluate amblyopia by narrowing the light beam and illuminating one eye at a time. Fixation with each eye should be steady on the light; if amblyopia is present, ﬁxation may waver or the eye may remain deviated in the presence of strabismus. Photoscreening is a sophisticated application of the red reﬂex test. The MTI photoscreener creates a Polaroid picture of the red reﬂex that allows assessment of media opacities and refractive errors (see Fig. 1-2). Although not as sensitive as a traditional eye examination, it is a useful screening tool for general practitioners.29,30

Pupillary Examination Normal pupil size varies with age. The newborn has small, miotic pupils that increase to an average diameter of 7 mm by age 12 to 13 and then gradually decrease again throughout life. Reaction to light in infants is often difﬁcult to assess due to the natural miosis and uncontrolled near response to the examination light. With careful observation, a small light response can be seen in addition to the near response, but care must be taken to not mistake one for the other. Older children should have the near response controlled as much as possible by a distance ﬁxation target. If the examination light is too bright, the child will close his eyes; when necessary, they must be held open to get an adequate exam. It is important to rule out an afferent pupillary defect, especially with unilateral visual loss or strabismus. The swinging ﬂashlight test is routinely used, as in adults, but care must be taken to aim the light directly into the pupil, especially in strabismus, or an artiﬁcial afferent defect may be produced because of incomplete retinal stimulation. It is important

16

handbook of pediatric strabismus and amblyopia

to remember that only dense amblyopia can produce an afferent defect and that even then it is barely detectable.31 Any afferent defect of signiﬁcance in a patient with presumed amblyopia must be investigated further.

Slit Lamp Examination Although most young children who cannot cooperate with a slit lamp examination can be adequately evaluated with a muscle light, at times more detailed examination is mandatory. There are several handheld slit lamps, which have the advantage of being portable and useful in examining supine patients. The disadvantages are their cost and somewhat limited resolution. They are not very good for assessing mild intraocular inﬂammation or subtle corneal abnormalities, but they are the best alternative. There are several other more readily available magniﬁers such as the direct and indirect ophthalmoscope, both of which can be focused on the anterior segment. Whichever source is used, the exam is still limited by the child’s resistance and movement, even while restrained. At times, sedation is required to obtain the necessary information. Often a child of 1 or 2 years will allow a quick look at the standard slit lamp; the key is to keep the light as dim as possible, have in mind what you most want to see, and look at that ﬁrst.

Intraocular Pressure Measurements Certain children are more prone to develop elevated intraocular pressure, and these patients must have accurate measurements. Such patients include aphakes, those with any anterior segment anomaly, those with orbital vascular lesions, or those on steroids. Most children under 3 years will not cooperate with routine applanation tonometry and they must be supine (sedated or restrained). There are several useful handheld tonometers. The original Schiotz tonometer is easy to use and read but often is too large for the infant eye. It has the advantage of being less sensitive to pressures induced by lids or extraocular muscles but is more affected by ocular rigidity, which tends to be lower in infants. The Perkins tonometer is an applanation device using ﬂuorescein and a split prism to assess the pressure. It is highly accurate at all ranges of pressure but requires some experience on the part of the examiner to read and is unreliable with an abnormal corneal surface. Contact must also be made directly

chapter 1: pediatric eye examination

17

on the cornea, which is often difﬁcult in a struggling child with a good Bell’s phenomenon. The Tonopen is easier to use and can obtain approximate readings off the sclera or an irregular cornea, but it is not accurate at high or low pressures, and it is difﬁcult to hear the tones that signal endpoint when the child is crying.23 The pneumotonometer is easy to use and does not require corneal contact, but the equipment is less portable than the other two. Struggling and crying both cause swings in the intraocular pressure, which must be taken into account, and pressures taken with a calm child are more accurate. Small infants who are drowsy will sometimes allow tonometry, especially if they are held in their mother’s arms and given a bottle or paciﬁer. Sedation may be necessary for truly accurate readings. Chloral hydrate has the advantage of not lowering the pressure, whereas inhalation anesthetics and Propofol can.3,25 If an exam under anesthesia is done, the pressure should be measured as soon as safely possible after induction because it will become artiﬁcially lower with time.13

Keratometry Assessment of corneal shape can be done qualitatively or quantitatively. Several conditions predispose to corneal astigmatism, which may be amblyogenic or require contact lens correction. Children with limbal dermoids or corneal scars may have poor retinoscopy reﬂexes, which make accurate assessment of astigmatism difﬁcult. Placido’s disc is a keratoscope that images a series of concentric light rings on the cornea. The reﬂected image can be used to assess the axis of astigmatism and corneal regularity. It is handheld and nonthreatening to most children but only gives a rough qualitative assessment. More accurate measurements must be obtained with a keratometer; this may require a sleeping or sedated infant to get accurate readings, and the standard keratometer can be mounted on a special bar to use with supine infants.35 Such measurements are helpful for contact lens ﬁtting. Alcon Corporation has produced a handheld keratometer that has been very helpful in the pediatric age group.

Dilatation and Cycloplegia Cycloplegia is essential to eliminate uncontrolled accommodation and adequately assess the refractive error in children. Several agents are available, but the adequacy of cycloplegia, not

18

handbook of pediatric strabismus and amblyopia

the maximal pupil dilatation, is most important. Tropicamide is not a strong enough cycloplegic for young children; instead, cyclopentolate, homatropine, or atropine should be used. Cyclopentolate has the most rapid onset and shortest duration and thus lends itself to clinic use. For most children, one drop each of cyclopentolate 1% in combination with phenylephrine 2.5% is adequate.2 Lighter pigmented eyes may only require one or two applications, whereas darkly pigmented eyes may require more than three. For children less than 6 months old, it is safer to use diluted drops such as Cyclomidril (cyclopentolate 0.2% and phenylephrine 1%). Homatropine 5% is another choice used for clinic dilation, especially in darkly pigmented patients, but this drop lasts up to 3 days. Both cyclopentolate and homatropine produce maximal cycloplegia within 30 min to 1 h, but the former recovers within 1 day. Table 1-3 lists the various agents available and their effects. If cycloplegia seems inadequate, based on either pupil size or changing retinoscopy streak, it is best to use atropine; this is usually given to the parents to take home and administer. To avoid toxicity of frequently administered atropine, the drops are given twice a day for 3 days prior to the visit.15 For infants and very young children, the drops should be given only once a day to each eye, with one eye receiving one drop in the morning and the other eye receiving one drop at night. As an alternative, atropine 0.5% could be used. Atropine should not be given to children with possible heart defects or reactive airways. Punctal occlusion can be performed for 1 min after the drops to decrease systemic absorption. Parents should be alerted to discontinue the drops if signs of toxicity or allergy develop (ﬂushing, tachycardia, fever, delirium, lid edema, redness of the eyes). Most cases of toxicity respond to discontinuation of the drops, but more severe cases can require treatment with subcutaneous physostigmine (Eserine), 0.25 mg every 15 min, until improvement occurs. This treatment is useful for toxicity with any of the antimuscarinic agents. The phenylephrine drops will occasionally cause blanching of the periocular skin, especially where the drop contacts the skin either by tears or a tissue; this is seen most often in infants and does not require treatment or discontinuation of the drops. For examination of premature babies, dilate with cyclomidril (combination of cyclopentolate and phenylephrine) and tropicamide 0.5%. Refraction is always an art, especially in a preverbal child. Care must be taken to control the working distance and the

0.5, 1, 2

2, 5

0.5, 1

Homatropine

Atropine

0.5, 1

Tropicamide

Cyclopentolate

2.5

Phenylephrine

Agent

Strength (%)

30–60

40–90

30–60

20–40

20

Maximum (min)

Mydriasis

7–14 days

1–3 days

6–24 h

2–6 h

2–3 h

Recovery time

TABLE 1-3. Cycloplegic/Mydriatic Agents in Children.

60–180

30–60

25–75

30

None

3–12 days

1–3 days

6–24 h

2–6 h

Recovery time

Cycloplegia Maximum (min)

Side effects

Flushing tachycardia, fever, delirium

Ataxia

Psychosis, seizure

Tachycardia, hypertension

chapter 1: pediatric eye examination

19

20

handbook of pediatric strabismus and amblyopia

visual axis, or inaccurate readings will be taken. Expertise with loose trial lenses or a skiascopy rack is important as the phoropter is useless in small children. If the endpoint is unclear, it is best to get a second or even third reading, either by repeat refraction on another visit or by a second refractionist. There are several handheld autorefractors on the market now that show promise in pediatric application (Nikon Retinomax, Welch Allyn Suresight).1,8,42 Cycloplegia may still be necessary to optimize results.

Fundus Examination An adequate fundus examination is imperative for all children who present to the ophthalmologist. The extent of the fundus exam necessary will vary widely depending on the patient. For most patients visualization of the posterior pole (optic nerve and macula) is adequate; this is done quickly and easily in most children by keeping the indirect light low and not touching the child. A brief look may be all that is obtainable by this technique, but this is often adequate. The optic nerve can be examined in more detail with the direct ophthalmoscope if the examiner is unhurried and stays several inches away from the child. By staying focused on the retinal vessels, the observer can see the nerve as it wanders into view while the child is busy watching a distant target (moving targets, especially videos, work best for this). For more detailed fundus examination or examination of the periphery, sedation or restraints are usually needed because most children will not tolerate the examining light for extended periods of time. As fundus examination comes at the end of the clinic visit, the child may be sleeping, especially if they have taken a bottle after the eyedrops, and this makes the examination much easier. Children less than 2 years old can usually be restrained adequately to allow a thorough fundus examination, even to the periphery, whereas older children require examination under anesthesia if uncooperative.

References 1. Adams RJ, et al. Noncycloplegic autorefraction in infants and young children (ARVO abstract 2108). Investig Ophthalmol Vis Sci 2001; 42. 2. Altman B. Drugs in pediatric ophthalmology. In: Harley RD (ed) Pediatric ophthalmology. Philadelphia: Saunders, 1983.

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3. Ausinsch B, Graves SA, Munson ES, Levy NS. Intraocular pressures in children during isoﬂurane and halothane anesthesia. Anesthesiology 1975;42:167. 4. Beazley ID, Illingworth DF, Jahn A, Greer DV. Contrast sensitivity in children and adults. Br J Ophthalmol 1980;64:863. 5. Birch J, Chisholm IA, Kimear P, et al. Clincal testing methods. In: Pokorney J, Smith VC, Verriest G, Pinckers AJLG (eds) Congenital and acquired color vision defects. New York: Grune & Stratton, 1979. 6. Boothe RG, Dobson V, Teller DY. Postnatal development of vision in human and nonhuman primates. Annu Rev Neurosci 1985;8:495. 7. Breton ME, Nelson LB. What do color blind children really see? Guidelines for clinical prescreening based on recent ﬁndings. Surv Ophthalmol 1983;27:306. 8. el-Defrawy S, Clarke WN, Belec F, Pham B. Evaluation of a handheld autorefractor in children younger than 6. J Pediatr Ophthalmol Strabismus 1998;5:107. 9. Fox et al. Use of high dose chloral hydrate for ophthalmic exams in children: a retrospective review of 302 cases. J Pediatr Ophthalmol Strabismus 1990;27:242. 10. Frankenburg WK, Dodds JB. The Denver developmental screening test. J Pediatr 1967;71:181. 11. Fulton AB, Hansen RM, Manning KA. Measuring visual acuity in infants. Surv Ophthalmol 1981;25:352. 12. Dickey CF, Metz HS, Stewart SA, Scott WE. The diagnosis of amblyopia in cross-ﬁxation. J Pediatr Ophthalmol Strabismus 1991;28:171. 13. Dominguez A, Banos MS, Alvarez G, et al. Intraocular pressure measurement in infants under general anesthesia. Am J Ophthalmol 1974; 78:10. 14. Dobson V, Teller DA. Visual acuity in human infants: a review and comparison of behavioral and electrophysiologic studies. Vision Res 1978;18:1469. 15. Gilman AG, Goodman LS, Gilman A. The pharmacological basis of therapeutics, 6th edn, 1980:11. 16. Glaser JS. Neuro-ophthalmologic examination: general considerations and special techniques. In: Glaser JS (ed) NeuroOphthalmology. Philadelphia: Lippincott, 1990. 17. Glaser JS. In: Glaser JS (ed) Neuro-Ophthalmology. Philadelphia: Lippincott, 1990. 18. Graf MH, Becker R, Kaufmann H. Lea Symbols: visual acuity assessment and detection of amblyopia. Graefe’s Arch Clin Exp Ophthalmol 2000;238:53. 19. Hered RW, Murphy S, Clanay M. Comparison of the HOTV and Lea Symbols chart for preschool vision screening. J Pediatr Ophthalmol Strabismus 1997;34:24. 20. Hess RF, Howell ER. The threshold contrast sensitivity function in strabismic amblyopia: evidence for a two type classiﬁcation. Vision Res 1977;17:1049.

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21. Hoyt CS, Nickel BL, Billson FA. Ophthalmological examination of the infant. Dev Aspects Surv Ophthalmol 1982;26:177. 22. Judisch GF, Anderson S, Bell WE. Chloral hydrate sedation as a substitute for examination under anesthesia in pediatric ophthalmology. Am J Ophthalmol 1980;89:560. 23. Kao SF, Lichter PR, Bergstrom TJ, et al. Clinical comparison of the oculab tonopen to the Goldmann applanation tonometer. Ophthalmology 1987;94:1541. 24. Koskela PU, Hyvarinen L. Contrast sensitivity in amblyopia. III. Effect of occlusion. Acta Ophthalmol 1986;64:386. 25. Laurelti GR, Laurelti CR, Laurelti-Filho A. Propofol decreases ocular pressure in outpatients undergoing trabeculectomy. J Clin Anesth 1997;9:289. 26. Mayer DL, Fulton AB, Rodier D. Grating and recognition acuities of pediatric patients. Ophthalmology 1984;91:947. 27. McDonald MA. Assessment of visual acuity in toddlers. Surv Ophthalmol 1986;31:189. 28. McMillan F, Forster RK. Comparison of MacKay-Marg, Goldmann, and Perkins tonometers in abnormal corneas. Arch Ophthalmol 1975;93:420. 29. Oher WL, Scolt WE, Holgado SI. Photoscreening for amblyogenic factors. J Pediatr Ophthamol Strabismus 1995;32:289. 30. Simons BD, Siathowski RM, Schiffmen JC, Berry BE, Flynn JJ. Pedatric photoscreening for strabismus and refractive errors and a highrisk population. Ophthalmology 1999;106:1073. 31. Portnoy JZ, Thompson HS, Lennarson L, Corbett JJ. Pupillary defects in amblyopia. Am J Ophthalmol 1983;96:609. 31a. Rogers GL, Bremer DL, Leguire LE. The contrast sensitivity function and childhood amblyopia. Am J Ophthalmol 1987;104:64. 32. Sokol S. Visually evoked potentials: theory, techniques and clinical applications. Surv Ophthalmol 1976;21:18. 33. Sokol S, Hansen VC, Moskowitz A, et al. Evoked potential and preferential looking estimates of visual acuity in pedatric patients. Ophthalmology 1983;90:552. 34. Stuart JQ, Burian HM. A study of separation difﬁculty: its relationship to visual acuity in normal and amblyopic eyes. Am J Ophthalmol 1962;53:471. 35. Szirth B, Matsumoto E, Murphree AL, Wright KW. Attachment for the Bausch and Lomb keratometer in pediatry. J Pediatr Ophthalmol Strabismus 1987;24:186. 36. Teller DY, Morse R, Borton R, Regan D. Visual acuity for vertical and diagonal gratings in human infants. Vision Res 1974;14:1433. 37. Terndrup TE, Cantor RM, Madden MD. Intramuscular meperidine, promethazine, and chlorpromazine: analysis of use and complications in 487 pediatric emergency department patients. Ann Emerg Med 1989;18:528. 38. Tongue AC, Cibis GW. Bruckner test. Ophthalmology 1981;88: 1041.

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39. von Noorden GK. Symptoms in heterophoria and heterotropia and psychologic effects of strabismus. In: Klein EA (ed) Binocular vision and ocular motility. St. Louis: Mosby, 1990. 40. Watcha MF, Chu FC, Stevens JL, Forestner JE. Effects of halothane on intraocular pressure in anesthetized children. Anesth Analg 1990; 71:181. 41. Weiner N. Atropine, scopolamine, and related antimuscarinic drugs. In: Gilman AG, Goodman LS, Gilman A (eds) The pharmacological basis of therapeutics, 6th edn. New York: Macmillan, 1980. 42. Wesemann W, Dick B. Accuracy and accommodation capability of a handheld autorefractor. J Cataract Refract Surg 2000;26:62. 43. Whitford AM, Hone SW, O’Hare B, Magner J, Eustace P. Intraocular pressure changes following laryngeal mask airway insertion: a comparative study. Anesthesia 1997;52:794. 44. Wright KW, Edelman PM, Walonker F, Yiu S. Reliability of ﬁxation preference testing in diagnosing amblyopia. Arch Ophthalmol 1986; 104:549–553. 45. Wright KW, Eriksen J, Shors TJ. Detection of amblyopia with P-VEP during chloral hydrate sedation. J Pediatr Ophthalmol Strabismus 1987;24:170–175. 46. Wright KW, Eriksen J, Shors TJ, Ary JP. Recording pattern visual evoked potentials under chloral hydrate sedation. Arch Ophthalmol 1986;104:718. 47. Wright KW, Walonker F, Edelman P. 10-diopter ﬁxation test for amblyopia. Arch Ophthalmol 1981;99:1242. 48. Zipf RF. Binocular ﬁxation pattern. Arch Ophthalmol 1976;94:401– 405.

2 Anatomy and Physiology of Eye Movements Kenneth W. Wright

OCULAR POSITION Within the orbit, the eye is suspended by six extraocular muscles (four rectus muscles and two oblique muscles), suspensory ligaments, and surrounding orbital fat (Fig. 2-1). A tug-of-war exists between the rectus and oblique muscles. The four rectus muscles insert anterior to the equator, and pull the eye posteriorly, while the two oblique muscles insert posterior to the equator providing anterior counterforces. Posterior orbital fat also pushes the eye forward. If rectus muscle tension increases, the eye will be pulled back causing enophthalmos and lid ﬁssure narrowing. Simultaneous cocontraction of the horizontal rectus muscles in Duane’s syndrome, for example, can cause signiﬁcant lid ﬁssure narrowing and enophthalmos. In contrast, decreased rectus muscle tone causes proptosis and lid ﬁssure widening. Conditions such as muscle palsies or a detached rectus muscle allow the eye to move forward and result in lid ﬁssure widening. Rectus muscle tightening procedures such as resections tend to cause lid ﬁssure narrowing whereas loosening procedures such as rectus recessions induce lid ﬁssure widening. When the eye is looking straight ahead with the visual axis parallel to the sagittal plane of the head, the eye is in primary position. The vertical rectus muscles follow the orbits and diverge from the central sagittal plane of the head by 23°. Thus, the visual axis in primary position is 23° nasal to the muscle axis of the vertical rectus muscles (Fig. 2-2). This discrepancy between the vertical rectus muscle axis and the visual axis of the eye explains the secondary and tertiary functions of the vertical rectus muscles (see muscle functions, following). 24

Whitnall's lig. Superior oblique m. Levator palpebrae Müller's m. Superior rectus m. Intraconal fat

Lateral rectus m. Inferior rectus m.

Lockwood's lig. Extraconal fat

Inferior oblique m.

FIGURE 2-1. Side view of extraocular muscles. Note that the rectus muscles pull the eye posteriorly while the oblique muscles pull the eye anteriorly.

FIGURE 2-2. Diagram shows visual axis versus muscle/orbital axis. Note that the visual axes parallel the central sagittal plane, while the orbital axis of each eye diverges 23° from the visual axis.

25

26

handbook of pediatric strabismus and amblyopia

The term position of rest refers to the position of the eyes when all the extraocular muscles are relaxed or paralyzed. Normally, the position of rest is divergent (i.e., exotropic), with the visual axis in line with the orbital axis. The eyes of a patient under general anesthesia are usually deviated in a divergent position.

OCULAR MOVEMENTS Ductions The term ductions is used to describe monocular eye movements without regard for the movement of the fellow eye (Fig. 2-3). Ductions result from an extraocular muscle contraction

A

B

E

C

F

D

G

FIGURE 2-3A–G. Diagram of ductions, which are monocular eye movements.

27

chapter 2: anatomy and physiology of eye movements

TABLE 2-1. Extraocular Muscles.

Muscle Medial rectus Lateral rectus Superior rectus

Approximate muscle length (mm) Origin 40 40 40

Annulus of Zinn Annulus of Zinn Annulus of Zinn

Anatomic insertion (mm)

Tendon Arc of length contact (mm) (mm)

Action from primary position

5.5

4

6

Adduction

7.0

8

10

Abduction

8.0

6

6.5

6.5

7

7

26

12

1

15

Inferior rectus

40

Annulus of Zinn

Superior oblique

32

Inferior oblique

37

Orbit apex From above temporal annulus pole of of Zinn superior rectus to within 6.5 mm of optic nerve Lacrimal Macular fossa area

Elevation Adduction Intorsion Depression Adduction Extorsion Intorsion Depression Abduction

Extorsion Elevation Abduction

that pulls the scleral insertion site toward the muscle’s origin while the opposing extraocular muscle simultaneously relaxes. The contracting muscle is referred to as the agonist and the relaxing muscle as the antagonist. An upward movement of an eye is referred to as supraduction or sursumduction, a downward movement is termed infraduction or dorsumduction, a nasal-ward movement is termed adduction, and a temporal movement is termed abduction. Torsional rotations (twisting movements) are known as cycloductions, with incycloduction (intorsion) referring to a nasal rotation of the 12 o’clock position of the cornea and excycloduction (extorsion) referring to a temporal rotation of the 12 o’clock position.

Muscle Action Versus Field of Action The terms “muscle action” and the “ﬁeld of action” are often confused. Muscle action refers to the effect of muscle contraction on the rotation of the eye when the eye starts in primary position. Table 2-1 lists the muscle actions of each extraocular muscle. Horizontal rectus muscles have but one action: horizontal rotation of the eye. Vertical rectus and oblique muscles,

28

handbook of pediatric strabismus and amblyopia

however, have three actions: vertical, horizontal, and torsional. The most robust action is termed the primary action, followed by the less obvious secondary and tertiary actions. It is important to remember the classic descriptions of primary, secondary and tertiary muscle actions as they relate to the eye when it is in primary position. In contrast, the ﬁeld of action of a muscle is the position of gaze when an individual muscle is the primary mover of the eye. Granted, virtually all eye movements are the result of combined contraction and relaxation of multiple muscles, but there are eight positions of gaze where one muscle provides the dominant force (Fig. 2-4). For example, when one looks up, the brain recruits both the superior rectus and the inferior oblique muscles. Looking up and nasal, however, is the primary function of the inferior oblique muscle, so this is the ﬁeld of action of the inferior oblique muscle. A muscle’s function is best evaluated by having the patient look into the ﬁeld of action of the

FIGURE 2-4. Diagram of the ﬁeld of action of the extraocular muscles. Arrows point to the quadrant where the speciﬁed muscle is the major mover of the eye. SR, superior rectus; IR, inferior oblique; MR, medial rectus; SO, superior oblique; IO, inferior oblique; IR, inferior rectus; LR, lateral rectus.

chapter 2: anatomy and physiology of eye movements

29

muscle. Thus, even though the secondary action of the inferior oblique muscle is abduction, evaluate inferior oblique function by having the patient look “up and nasal.” A patient with an inferior oblique palsy will show limitation of eye movement up and nasal. Note, for straight upgaze, the superior rectus muscle is the major elevator, and for straight down-gaze the inferior rectus is the major depressor, with the oblique muscles contributing little.

Smooth Pursuit Versus Saccadic Eye Movements There are two basic forms of eye movements: smooth pursuit and saccadic. Smooth pursuit eye movements are generated in the occipital parietal temporal cortex, with the right cortex controlling movements to the right and the left cortex controlling movements to the left. In humans, smooth pursuit ﬁrst occurs at 4 to 6 weeks of age. These are slow accurate eye movements requiring visual feedback from central foveal ﬁxation. Smooth pursuit eye movements can follow visual targets moving at velocities up to 30° per second (30°/s). Clinically, accurate smooth pursuit indicates central ﬁxation and in preverbal children is an indication of good vision. Saccadic movements are rapid eye movements with velocities usually ranging from 200° to 700°/s, but saccades have been recorded up to 1000°/s. The peak velocity increases as the amplitude of the movement increases, and this relationship is termed the main sequence. Saccades are movements used to keep up with targets moving too fast for smooth pursuit and for quick reﬁxation from one target to another. Saccadic eye movements develop before smooth pursuits, occurring as early as 1 week of age. Saccadic eye movements are generated in the frontal lobes and are under contralateral control; that is, right frontal lobe stimulation will result in a saccadic eye movement to the left. Saccadic movements can be voluntarily initiated, but they are not voluntarily controlled, and there is no signiﬁcant visual feedback to adjust the amount of movement. It is thought that the amplitude of a saccadic movement is preprogrammed based on the degree of retinal eccentricity of the target; this is why saccadic movements are termed ballistic, analogous to the ballistic trajectory of a cannon ball. The neuronal signal that initiates a saccade consists of a burst of high-frequency discharge or pulse to the agonist and inhibition of the antagonist. Because all neurons available are activated for eye movements greater than

30

handbook of pediatric strabismus and amblyopia

5°, the magnitude of a saccade is determined by the duration of the pulse. At the end of a saccade, tonic neuronal ﬁring of the agonist and antagonist muscles occurs to hold the eye position referred to as the step. Vision during a saccadic eye movement is suspended or suppressed. Some have used the term saccadic omission for the process of cortical suppression.1 A tremendous force is required to produce a saccadic eye movement; therefore, the presence of saccadic eye movements indicates “good” muscle function. Only rectus muscles generate saccadic eye movements. When evaluating a patient with limited ductions, look for the presence of a normal saccadic eye movement into the ﬁeld of limited ductions. If there is a brisk saccade in the direction of the limitation, this indicates good muscle function and suggests the limited movement is caused by restriction, not a muscle paresis. Optokinetic nystagmus (OKN) can be generated by a slowly rotating drum with stripes and used to evaluate smooth pursuit and saccadic eye movements. As the drum rotates toward the patient’s right, there is a smooth pursuit eye movement to the right to follow the stripe. As the end of the stripe passes, there is a fast saccadic movement to the left to reﬁxate on the next stripe. At target velocities less than 30°/s, smooth pursuit keeps pace with the target. At velocities between 30° and 100°/s, smooth pursuit movements progressively lag behind the target. At velocities greater than 100°/s, OKN is not evoked. OKN can be used to evaluate saccadic and smooth pursuit eye movements. Look at the fast phase of OKN to evaluate saccadic movements and the slow phase to evaluate smooth pursuit.

ANATOMY OF THE EYE MUSCLES Rectus Muscles The four rectus muscles originate at the orbital apex at the annulus of Zinn and course anteriorly to insert on the anterior aspect of the globe. The “straight” course of the rectus muscles gives rise to the term rectus. The rectus muscle insertions form a progressive spiral termed the spiral of Tillaux around the corneal limbus. The medial rectus muscle is the closest to the limbus (5.5 mm), then the inferior rectus (at 6.5 mm), the lateral rectus (at 7.0 mm), and the superior rectus is the furthest from the limbus (8.0 mm). The muscle–scleral insertion line has

chapter 2: anatomy and physiology of eye movements

31

FIGURE 2-5. Diagram of distance of the rectus muscle insertions from the limbus (in millimeters, mm). Note that the medial rectus muscle inserts closest to the limbus and the distances increase, going counterclockwise from the medial rectus toward the superior rectus, which inserts furthest from the limbus.

a horseshoe conﬁguration with the rounded apex pointing toward the cornea (Fig. 2-5). One can remember this as the horseshoes are always galloping toward the cornea. The scleral thickness behind the rectus insertions is the thinnest of the eye, being only 0.3 mm thick. Hooking a rectus muscle requires passing the hook several millimeters behind the central muscle insertion to clear the posterior aspect of the horseshoe insertion. The widths of the insertions are all approximately 10 mm, and the distance between insertions or intermuscle spacing is only 6 to 8 mm. Because of the proximity of the rectus muscle insertions, it is easier than you might think to hook the wrong muscle during strabismus surgery. An important number to remember is the rectus muscle length, which is 40 mm for all rectus muscles and is also the length of the orbit. Rectus muscles are innervated from the intraconal side of the muscle belly at the junction of the anterior two-thirds and posterior one-third of the muscle.

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handbook of pediatric strabismus and amblyopia

HORIZONTAL RECTUS MUSCLES The horizontal rectus muscles consist of the medial and lateral rectus muscles. In primary position, each muscle has one action: the medial rectus is an adductor and the lateral rectus is an abductor (Fig. 2-6). When the eye elevates or depresses away from primary position, however, the horizontal rectus muscles take on secondary vertical functions. When the eye is “up,” the horizontal rectus muscles take on a secondary action of supraduction, and when the eye is “down,” the secondary action is infraduction (Fig. 2-7). In addition, if one surgically transposes a horizontal rectus muscle insertion up, the muscle becomes an elevator in addition to the horizontal function. Supraplacing the horizontal rectus insertions during strabismus surgery will induce a hyperdeviation whereas infraplacement induces a hypodeviation. Vertically displacing the medial and lateral rectus muscle insertion is an excellent way to correct small vertical deviations when performing a recession/resection procedure. In Duane’s syndrome, the common ﬁnding of upshoot and downshoot is probably caused by the secondary elevator and depressor actions of the cocontracting horizontal rectus

FIGURE 2-6. Diagram of simple function of the medial rectus (MR) and lateral rectus (LR) muscle with the eye in primary position.

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A

B

C FIGURE 2-7A–C. Diagram of secondary actions of the medial rectus when the eye rotates up or down. These secondary actions also relate to the lateral rectus. (A) Globe rotated superiorly; now the medial rectus acts as an elevator in addition to its adduction or horizontal function. (B) In the center part of the ﬁgure, the medial rectus is a pure adductor. (C) Globe rotated down; in this position, the medial rectus acts as a depressor and an adductor.

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handbook of pediatric strabismus and amblyopia

muscles. Remember, the secondary vertical functions of the horizontal rectus muscles occur only when the eye is rotated vertically off primary position.

MEDIAL RECTUS MUSCLE The medial rectus muscle is innervated by the lower division of the oculomotor nerve (third cranial nerve) and, in primary position, is a pure adductor. The medial rectus is uniquely diminutive. It has the shortest arc of scleral contact (6 mm) and the shortest tendon length of the rectus muscles (4 mm). The inferior oblique muscle actually has the shortest tendon (1 mm) of the extraocular muscles, but it is not a rectus muscle. (Be careful; this could be the basis of a trick question.) Of the extraocular muscles, the medial rectus inserts closest to the limbus and is therefore susceptible to insult during anterior segment surgical procedures. Inadvertent removal of the medial rectus muscle is a well-known complication of pterygium removal. The medial rectus is also unique, as it is the only rectus muscle without fascial connections to an adjacent oblique muscle. This lack of oblique muscle connection makes the medial rectus the most difﬁcult to surgically retrieve if lost. Once disinserted, the medial rectus is free to retract completely off the globe into the orbital fat, making retrieval extremely difﬁcult and, in some cases, almost impossible.

LATERAL RECTUS MUSCLE The lateral rectus muscle is innervated by the sixth cranial nerve and is a pure abductor. In direct contrast to the medial rectus muscle, the lateral rectus has the longest tendon (8 mm) and the longest arc of scleral contact (10 mm) of the rectus muscles. Be careful, the “longest” cited above refers to only rectus muscles, as the superior oblique tendon has the longest arc of contact and tendon length of all the extraocular muscles. (This could be the source of another trick question.) The long arc of contact occurs because the lateral rectus muscle initially has a divergent course following the lateral wall of the orbit. Then, in the anterior orbit, it turns nasally, wrapping around the globe to its scleral insertion point (see Fig. 2-6). This temporal to nasal wrap around the globe accounts for the long arc of contact. The inferior border of the lateral rectus muscle courses above the inferior oblique insertion, and there are connective tissue bands connecting the lateral rectus muscle to the inferior oblique muscle.13 This is an important anatomic relationship, because a lost lateral rectus

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muscle will come to rest at the insertion of the inferior oblique muscle. The surgeon can often ﬁnd a lost lateral rectus muscle by tracing the inferior oblique muscle back to its insertion.

VERTICAL RECTUS MUSCLES

EA XIS

VISUAL AXIS

The superior and inferior rectus muscles are the vertical rectus muscles and are the major elevators and depressors of the eye, respectively. The vertical rectus muscles have secondary and tertiary actions because, in primary position, the muscle axis is 23° temporal to the visual axis of the eye (Figs. 2-2, 2-8A).

MU

SC L

23°

TEMPORAL VI MUSUA SC L & LE A

XIS

NASAL

MU SC LE

AX IS

A

B

VISUAL AXIS

C FIGURE 2-8A–C. Functions of the vertical rectus muscles with the eye in various positions of gaze. (A) The eye is in primary position with the visual axis 23° nasal to the muscle axis. (B) The eye is abducted 23° from the primary position, and the visual axis is in line with the muscle axis. (C) The eye is abducted more than 23° from the primary position, and the visual axis is now temporal to the muscle axis.

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handbook of pediatric strabismus and amblyopia

Their secondary action is adduction, and it occurs because the vertical rectus muscles pull the front of the eye nasal to the visual axis. Tertiary actions are torsional, consisting of intorsion for the superior rectus muscle and extorsion for the inferior rectus muscle. These secondary and tertiary muscle actions are dependent on eye position. If the eye is abducted 23°, for example, the muscle and visual axes will be in line, and the vertical rectus muscles lose their secondary and tertiary actions, leaving only their vertical actions (Fig. 2-8B). In this position of 23° abduction, the superior rectus acts purely as an elevator, and the inferior rectus purely as a depressor. With further abduction past 23°, the secondary and tertiary actions of the vertical rectus muscles return, but they are different. The secondary action for both vertical rectus muscles becomes abduction, and the tertiary functions reverse, becoming extorsion for the superior rectus and intorsion for the inferior rectus muscle (Fig. 2-8C).

SUPERIOR RECTUS MUSCLE The upper division of the oculomotor nerve innervates the superior rectus muscle. It is the major elevator of the eye, and its actions include supraduction (primary), adduction (secondary), and intorsion (tertiary). The superior rectus muscle overlies the superior oblique tendon and has connective tissue connections to the superior oblique tendon below and the levator palpebrae muscle above (Fig. 2-9). This anatomic relationship to the levator palpebrae is important because a large superior rectus recession can cause upper lid retraction and lid ﬁssure widening. On the other hand, a superior rectus resection pulls the upper lid down, resulting in lid ﬁssure narrowing. Lid ﬁssure changes associated with superior rectus surgery can be minimized by surgically removing the fascial connections between the levator and the superior rectus muscles.

INFERIOR RECTUS MUSCLE The inferior rectus muscle is innervated by the lower division of the oculomotor nerve and is the principal depressor of the eye. Actions of the inferior rectus muscle include infraduction (primary), adduction (secondary), and extorsion (tertiary). The inferior rectus is sandwiched between the inferior oblique below

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FIGURE 2-9. Diagram of the eye and orbit from a top view looking down on the superior rectus (SR) muscle. Note that the superior rectus muscle overlies the superior oblique (SO). T, temporal; N, nasal.

and the sclera above (Fig. 2-10). The fascial connection between the inferior rectus muscle, the inferior oblique muscle, and the lower lid retractors (capsulopalpebral fascia) is termed Lockwood’s ligament (Fig. 2-11).17 These fascial connections are responsible for the eyelid changes that often occur after inferior rectus surgery. An inferior rectus recession results in lower lid retraction with lid ﬁssure widening, and a resection causes lid advancement with lid ﬁssure narrowing. If the inferior rectus is inadvertently disinserted or lost during surgery, these connections will hold the inferior rectus to the inferior oblique and keep it from retracting posteriorly. The surgeon who is in search of a lost inferior rectus muscle can usually ﬁnd it lying between the inferior oblique and sclera.

FIGURE 2-10. Diagram of the eye and orbit viewed from below. Note that the inferior oblique (IO) underlies the inferior rectus (IR) muscle.

Conjunctiva Tarsus

Fornix Tenon's capsule

Orbicularis m.

Inf. rectus m.

ITM CPF Orbital septum CPH Lockwood's lig. Inf. oblique m.

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FIGURE 2-12. Diagram of the superior oblique (SO) muscle and tendon. The functional muscle axis extends from the trochlea to the superior oblique insertion. The muscle axis is 54° nasal to the visual axis.

OBLIQUE MUSCLES Like the vertical rectus muscles, the oblique muscles have primary, secondary and tertiary actions. In the case of the oblique muscles, this is because the functional muscle axis is approximately 50° nasal to the visual axis, and the insertion extends posterior to the equator of the eye (Figs. 2-12, 2-13). By

FIGURE 2-11. Diagram of the relationship between the inferior rectus, inferior oblique, lower lid retractors, and Lockwood’s ligament. The inferior tarsal muscle (ITM) courses from the posterior border of the tarsus toward the inferior oblique muscle. It then passes between the inferior oblique muscle and the inferior rectus muscle to insert at the capsulopalpebral head (CPH). The CPH extends posteriorly to connect the inferior oblique to the inferior rectus muscle. The capsulopalpebral fascia (CPF) is the anterior extension of the CPH and courses from the inferior oblique anteriorly to the tarsus along with the ITM. “Lockwood’s ligament” (Lockwood’s lig.) consists of these fascial attachments that connect the lower lid, inferior rectus, and inferior oblique muscles.

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handbook of pediatric strabismus and amblyopia

FIGURE 2-13. Diagram of the inferior oblique (IO) from a view from below. The inferior oblique muscle axis is 51° nasal to the visual axis.

comparing Figures 2-12 and 2-13, one can see that the oblique muscles have an almost identical functional course with both muscle axes at approximately 50°. The posterior muscle–scleral insertion gives the oblique muscles their seemingly paradoxical vertical functions, with the superior oblique being a depressor and the inferior oblique an elevator. The oblique muscles have no anterior ciliary blood supply, and they do not contribute to the anterior segment circulation. Remember that the “oblique muscles always course below the corresponding vertical rectus muscle” (Fig. 2-14).

SUPERIOR OBLIQUE MUSCLE The primary action of the superior oblique muscle is intorsion, but it also acts as a depressor (secondary) and an abductor (tertiary). Depression and abduction occur as the back of the eye is pulled up and in toward the trochlea. The superior oblique

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muscle originates at the orbital apex just above the annulus of Zinn and gradually becomes tendon at the trochlea (see Fig. 2-12). After passing through the trochlea, the superior oblique tendon reverses course and turns in a posterior temporal direction to pass under the superior rectus muscle to insert on sclera along the temporal border of the superior rectus muscle (Fig. 2-14). Even though the anatomic origin is at the apex of the orbit, the functional origin of the superior oblique is at the trochlea. This tendon is the longest tendon of the extraocular muscles, 26 mm in length. The tendon insertion fans out broadly under the superior rectus muscle, extending from the temporal pole of the superior rectus muscle to 6.5 mm from the optic nerve.13 Fascial attachments connect the superior oblique tendon to the superior rectus muscle above and to the sclera below.13 The tendon insertion can be functionally divided into two basic parts: the anterior one-third and the posterior two-thirds. Posterior ﬁbers are responsible for depression and abduction whereas tendon ﬁbers anterior to the equator are devoted to intorsion. This distinction between anterior and posterior superior oblique tendon ﬁbers is important because one can

FIGURE 2-14. Diagram of posterior anatomy of the eye and muscles. Note the proximity of the inferior oblique to the macula and vortex veins (vv). The posterior aspect of the superior oblique insertion is in proximity to the superior temporal vortex vein and is approximately 6 to 8 mm from the optic nerve.

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handbook of pediatric strabismus and amblyopia

manipulate these functions surgically to correct speciﬁc motility disorders. The Harada–Ito procedure, for example, involves tightening the anterior ﬁbers of the superior oblique tendon. Because the anterior tendon ﬁbers intort the eye, the Harada–Ito procedure can be used to treat extorsion associated with superior oblique palsy. The trochlear nerve innervates the superior oblique muscle at its midpoint from outside the muscle cone. The superior oblique muscle is, in fact, the only eye muscle innervated on the outer surface of the muscle belly. This unique innervation explains why a retrobulbar anesthetic block results in akinesia of all the eye muscles except the superior oblique muscle.

TROCHLEA The trochlea (Latin for pulley) is a cartilaginous U-shaped structure attached to the periosteum that overlies the trochlear fossa of the frontal bone in the superior nasal quadrant of the orbit. It has been taught that the superior oblique tendon moves through the trochlea much like a rope through a pulley. Anatomic studies have shown, however, that tendon movement is not that simple. Within the trochlea is a connective tissue capsule with connective tissue bands that unite the superior oblique tendon to the surrounding trochlea (Fig. 2-15).46 Some of the tendon slackening distal to the trochlea may come from a telescoping elongation of the central tendon (Fig. 2-16).19 This telescoping elongation of the tendon appears to be caused by movement of the central tendon ﬁbers that have scant interﬁber connections. Thus, the mechanism for tendon movement is complex, with at least two mechanisms: (1) tendon movement through the trochlea (pulley and a rope) and (2) tendon elongation (telescoping).

INFERIOR OBLIQUE MUSCLE It is the principal extortor of the eye; however, other actions include elevation (secondary) and abduction (tertiary). The inferior oblique muscle originates at the lacrimal fossa located at the anterior aspect of the inferior nasal quadrant of the orbit (see Fig. 2-13). Starting at the lacrimal fossa, the inferior oblique muscle courses posteriorly and temporally underneath the inferior rectus muscle to its scleral insertion, which is adjacent to the inferior border of the lateral rectus muscle (see Fig. 2-14). The inferior oblique muscle has fascial connections to the lower

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A

B FIGURE 2-15A–B. Histology of the trochlea. (A) Low-magniﬁcation cross section of midtrochlea. H&E stain. Note horseshoe shape of cartilaginous tissue and the ﬁbrous connective tissue ring that surrounds the superior oblique muscle. At this cross section, the superior oblique is two-thirds muscle and one-third tendon. (B) High-magniﬁcation cross section of superior oblique muscle in midtrochlea shows ﬁbrous connective tissue ring connecting to muscle via ﬁne fascial septae.

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handbook of pediatric strabismus and amblyopia

C

D FIGURE 2-15C–D. (C) Low-magniﬁcation cross section of superior oblique tendon exiting the trochlea. Note small area of cartilage and larger ring of ﬁbrous connective tissue that surrounds the superior oblique tendon as the tendon capsule. At this section, the superior oblique is onethird muscle and two-thirds tendon. (D) High magniﬁcation of the superior oblique tendon exiting the trochlea. Note the superior oblique tendon capsule consists of circumferential onionskin layers of ﬁbrous connective tissue. The tendon capsule is attached to the superior oblique tendon capsule by circumferential connective tissue ﬁbers. (From Wright et al., Ref. 46, with permission.)

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FIGURE 2-16. Diagram of anatomy of the trochlea. Note the central ﬁbers of the tendon expand and retract more than the peripheral tendon ﬁbers. (From Ref. 19, with permission.)

border of the lateral rectus muscle and to the overlying inferior rectus muscle via Lockwood’s ligament (see Fig. 2-11). When the inferior oblique muscle contracts, it pulls the back of the eye down and in toward the insertion at the lacrimal fossa. This action produces elevation, abduction, and extorsion (Fig. 2-14). Important structures near the inferior oblique insertion include the macula and inferior temporal vortex vein (Fig. 2-14). The inferior oblique muscle has only 1 mm of tendon at its insertion. The inferior oblique muscle is innervated by the inferior branch of the third nerve at a point just lateral to the inferior rectus muscle. Innervation occurs at the posterior aspect of the inferior oblique muscle belly, and the nerve is accompanied by blood vessels forming a neurovascular bundle. This neurovascular bundle is surrounded by an inelastic capsule of collagen tissue that protects the inferior oblique nerve from damage caused by stretching.39 The neurovascular bundle with its insertion into the posterior aspect of the muscle is an important structure in regard to inferior oblique surgery. Anterior transposition of the inferior oblique muscle is an effective surgical

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handbook of pediatric strabismus and amblyopia

procedure used to treat inferior oblique muscle overaction; however, the complication of postoperative limited elevation has been reported.5,25,26,47 This complication is caused by anteriorizing the posterior muscle ﬁbers at, or anterior to, the inferior rectus muscle insertion, because this tightens the inelastic neurovascular bundle.38 The tight neurovascular bundle acts as the functional origin of the inferior oblique muscle and changes the action of the inferior oblique muscle from an elevator to a depressor (Fig. 2-17A).16 This author has coined the term J-deformity for this acute bend of the anteriorized inferior oblique.47 When the patient looks up, the inferior oblique muscle contracts along with the superior rectus muscle, but the anteri-

Inferior oblique muscle

Neurofibrovascular bundle

Maxillary bone

Inferior rectus muscle

FIGURE 2-17A,B. (A) Diagram of inferior oblique muscle anteriorization with “J-deformity.” The J-deformity is caused by anterior placement of the posterior inferior oblique muscle ﬁbers to the level of the inferior rectus muscle insertion. Because the neurovascular bundle of the inferior oblique muscle inserts in the posterior muscle belly, anteriorization of the posterior muscle ﬁbers produces a tight neurovascular bundle; this causes limited elevation of the eye as active contraction of the anteriorized inferior oblique muscle pulls against the tight neurovascular bundle.16

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Vortex vein Inferior oblique muscle

Inferior rectus muscle

FIGURE 2-17A,B. (B) Diagram of the “graded anteriorization” technique described by Guemes and Wright that is effective in reducing inferior oblique overaction but avoids the postoperative complication of limited elevation.16 The new inferior oblique muscle insertion is shown being placed 1 mm behind the inferior rectus muscle insertion, and the posterior muscle ﬁbers are placed an additional 4 to 5 mm further posterior, and parallel to the inferior rectus muscle axis. Note that the posterior placement of the posterior muscle ﬁbers avoids the J-deformity. By keeping the posterior muscle ﬁbers posterior to the anterior ﬁbers and avoiding the J-deformity, the neurovascular bundle remains loose, preventing postoperative limitation of elevation.

orized inferior oblique muscle now depresses the eye and limits elevation; this is an active leash caused by inferior oblique contraction, and forced ductions on patients with this complication of limited elevation often show only slight restriction to supraduction. The complication of limited elevation can be avoided while maintaining excellent results by anterior transposition of the anterior muscle ﬁbers at, or a millimeter or two behind, the inferior rectus insertion. Be sure to keep the posterior ﬁbers back, behind the anterior ﬁbers. Placing the posterior muscle ﬁbers several millimeters posterior to the inferior rectus insertion and in line with the inferior rectus muscle prevents the J-deformity (Fig. 2-17B).16,47

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handbook of pediatric strabismus and amblyopia

EXTRAOCULAR MUSCLE HISTOLOGY As are other skeletal muscles, extraocular muscles are made up of striated ﬁbers that, on electron microscopy, show the typical banding pattern of sarcomeres with overlapping threads of actin and myosin. Also resembling other muscles, the strength of an extraocular muscle contraction is dependent on the number of motor units activated (recruitment) and the frequency of muscle ﬁber stimulation. Extraocular muscles, however, do show some interesting anatomic and physiological differences from other skeletal muscles. The ﬁbers are variable in size, are considerably smaller, and contract more than 10 times faster than other skeletal muscle. Extraocular muscle ﬁbers are innervated at a high nerve ﬁber to muscle ﬁber ratio (almost 1:1), whereas other skeletal muscle can have up to 100 muscle ﬁbers for every nerve ﬁber. This rich innervation, teamed with a fast muscle reaction time, contributes to the precision, accuracy, and control of eye movements. Another distinction of extraocular muscles is the presence of two distinct muscle ﬁber types: fast muscle ﬁbers and slow muscle ﬁbers. The fast, or twitch, ﬁbers are single innervated ﬁbers (SIF), innervated by a large motor neuron with “en plaque” neuromuscular junctions and are typical of mammalian skeletal muscle. The SIF can be classiﬁed into three types: red, intermediate, and white. Red SIF have the highest density of mitochondria and are the most fatigue resistant, while the white SIF have fewer mitochondria and are less resistant to fatigue. Intermediate and white ﬁbers provide the high transient force needed for the extremely fast saccadic eye movements. Slow, or tonic muscle ﬁbers, are multiple innervated ﬁbers (MIF) innervated by small-diameter motor nerves with “en grappe” neuromuscular endings characteristic of avian and amphibian muscles. MIF are thought to participate in smooth pursuit movements and static muscle tone to hold and maintain eye position, and SIF probably also play a supportive role in tonic control of eye position and pursuit eye movements. The exact functions of the variety of speciﬁc muscle ﬁber types are unknown, and it is likely that various ﬁbers have overlapping functions.28 Within extraocular muscle tissue are neuromuscular spindles that are concentrated at the muscle–tendon junction. Neuromuscular spindles are thought to be sensory organs providing information on muscle tone to the brain.9 The exact role

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of the muscle spindles is unknown, but they may provide proprioceptive feedback to motor centers in the brain regarding muscle tone and eye position. Muscle spindles may explain why many adult patients experience transient spatial disorientation after strabismus surgery on the dominant eye.

ARCHITECTURE OF THE EXTRAOCULAR MUSCLES AND PULLEYS Extraocular muscles have two distinct muscle layers seen on transverse sections (cross section). There is a peripheral layer closest to the orbital wall called the orbital layer (OL) and an inner layer closest to the eye globe called the global layer (GL).33,37 OL muscle ﬁbers contain small-diameter ﬁbers with many mitochondria and abundant vessels, staining dark red by Masson’s trichrome. The GL, in contrast, contains larger ﬁbers with variable numbers of mitochondria and fewer vessels; it stains bright red by Masson’s trichrome. Approximately 90% of GL muscle ﬁbers are fast-twitch SIF, with one-third of the SIF being fatigue-resistant red SIF; 80% of OL muscle ﬁbers are twitch-generating SIF and 20% are MIF.33 In humans, OL muscle ﬁbers do not appear to run the entire course of the muscle and do not insert in sclera, as there is a gradual decline in the OL in the anterior aspect of the muscle.11,28 Elastic ﬁbers connect the OL to a ﬁbromuscular pulley sleeve that surrounds each extraocular muscle close to the muscle insertion (see Muscle Pulleys, following) (Fig. 2-18).11 There are also muscle-to-muscle-ﬁber junctions (myomyous junctions) within the OL. GL ﬁbers, on the other hand, are continuous from their origin in the orbital apex to their insertion by tendon into sclera.28 Most GL ﬁbers act in saccadic eye movements and function only in the ﬁeld of action of the muscle whereas OL ﬁbers are active throughout the oculomotor range, providing continuous muscle tone to the pulley system.7 Collins hypothesized that OL muscle ﬁbers might have a role in maintaining ﬁxation whereas GL muscle ﬁbers participate in dynamic eye movements.7 An alternative hypothesis proposed by Demer is that OL muscle ﬁbers actively control pulley position, thereby inﬂuencing the rotational force vectors during eye movements.11,28

A FIGURE 2-18A–C. Masson’s trichrome stain of 10-␮m-thick transverse section of medial rectus at the level of the pulley ring of a 17-month-old human. (A) Low power shows the overall architecture of the pulley (P) that surrounds the medial rectus muscle. Fibers in the orbital layer (OL) (arrowheads) insert in the pulley, shown at high power in (B). The OL muscle layer takes the form of a C-shape and is on the left, delineated by the large arrows; the global layer (GL) ﬁbers are to the right. OL on the left is shown on the bottom.

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51

B

C FIGURE 2-18A–C. (B) High-power magniﬁcation shows the insertion of the OL into the pulley (taken from the upper left box on A). (C) Highpower magniﬁcation of the GL and pulley relationship. The GL does not insert into the surrounding pulley (taken from the middle right box on A).11,28

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handbook of pediatric strabismus and amblyopia

EXTRAOCULAR MUSCLE FASCIA A smooth white connective tissue, Tenon’s capsule, underlies the conjunctiva and envelops the globe and extraocular muscles. This delicate membrane partitions the orbital contents, isolating the globe and extraocular muscles from the surrounding orbital fat. Another fascial structure interconnected with Tenon’s capsule is the muscle sleeve or extraocular muscle pulley, which suspends the extraocular muscles.

Muscle Pulley (Muscle Sleeve) Each of the rectus muscles passes through a pulley system consisting of a sleeve or ring of collagen, elastic, and smooth muscle ﬁbers. Previously, this structure was termed muscle sleeve. The medial rectus muscle pulley has the most ﬁbroelastic tissue and smooth muscle. Muscle pulleys connect to the orbital layer (OL) of the rectus muscle, to the orbital wall, to adjacent extraocular muscles, and to Tenon’s capsule.10 The pulley or sleeve extends for approximately 10 mm from the equator of the globe anteriorly to approximately 6 mm from the muscle insertion. During strabismus surgery, one can see these bands as they connect the surrounding muscle sleeve or pulley to the OL of the rectus muscle. Similar to the trochlea and superior oblique tendon, the pulleys guide the rectus muscles to their insertion point. In contrast to the superior oblique muscle, which changes direction after passing through the trochlea, rectus muscle pulleys keep the muscle in line with their anatomic origin. Demer has suggested that in secondary gaze positions the extraocular muscle path is “discretely inﬂected by the pulley.”6 Demer et al. also hypothesized that OL muscle ﬁbers insert into the pulley system and actively inﬂuence pulley position and the mechanics of ocular rotation.11,28

Tenon’s Capsule Tenon’s capsule is a collagen-elastic tissue that is a continuous membrane surrounding the eye and extraocular muscles.22 This membrane separates surrounding orbital fat from the globe and extraocular muscles. The elastic nature of Tenon’s capsule allows free rotation of the globe and unrestricted muscle relaxation and contraction. For clinical and surgical purposes, it is useful to subdivide it into the following categories:

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1. Intermuscular septum 2. Anterior Tenon’s capsule 3. Posterior Tenon’s capsule 4. Check ligaments 5. Muscle sleeve (see Pulley System, earlier)

INTERMUSCULAR SEPTUM This thin tissue lies sandwiched between the conjunctiva and sclera, spanning between the rectus muscles (Fig. 2-19).30,40 During strabismus surgery, intermuscular septum can be identiﬁed as the white membrane on each side of the rectus muscles. When elevated with muscle hooks, the intermuscular septum takes on the appearance of the wings of a manta ray (Fig. 2-20).45 The intermuscular septum can be safely incised during strabismus surgery, as it is not a barrier to orbital fat.

ANTERIOR TENON’S CAPSULE This tissue is the subconjunctival membrane anterior to the muscle insertions. It proceeds forward with the intermuscular septum and fuses with the conjunctiva at 2 to 3 mm posterior to the corneal limbus (Figs. 2-18, 2-20). When suturing a muscle during strabismus surgery, it is important to dissect anterior Tenon’s capsule off the tendon insertion to avoid the complica-

Reflected conjunctiva

SR IMS IMS

MR

LR

Anterior Tenon's Capsule FIGURE 2-19. Anterior ocular fascia. Intermuscular septum (IMS) is the connective tissue that spans between the rectus muscles underneath the conjunctiva. Anterior Tenon’s is that tissue anterior to the rectus muscle insertions; it fuses with the conjunctiva 3 mm posterior to the limbus.

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handbook of pediatric strabismus and amblyopia

A

B FIGURE 2-20A,B. (A) Lateral rectus muscle with intermuscular septum and check ligaments. Check ligaments overlie the rectus muscle and connect the muscle to the overlying conjunctiva. Intermuscular septum is seen on either side of the lateral rectus muscle, spanning between the superior and inferior rectus muscles. (B) Photograph shows the Jameson hook under the lateral rectus muscle and Desmarres retractor pulling the conjunctiva posteriorly. (Figure published with permission of J.B. Lippincott Co. from Wright KW. Color Atlas of Ophthalmic Surgery: Strabismus. Philadelphia: Lippincott, 1991.)

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Anterior Tenon's capsule

Medial rectus Anterior ciliary muscle artery FIGURE 2-21. Anterior Tenon’s capsule is the white tissue retracted anteriorly with a small Steven’s hook (bottom left hook). During strabismus surgery, it is important to remove the anterior Tenon’s capsule to visualize the muscle tendon for suturing. Note the anterior ciliary vessels on the tendon insertion.

tion of a slipped muscle (Fig. 2-21). If anterior Tenon’s capsule is left on the tendon, the surgeon may inadvertently suture and secure anterior Tenon’s capsule, missing all or part of the tendon. The unsuspecting surgeon then disinserts the unsutured tendon and allows the muscle to slip posteriorly while anterior Tenon’s capsule is placed at the intended recession site.31 A slipped muscle is a frequent cause of unexpected overcorrection after recession procedures, as it often goes unrecognized at the time of surgery. Remember that some slipped muscles involve only part of the muscle and can present as a mild overcorrection with relatively good muscle function.48

POSTERIOR TENON’S CAPSULE This tissue lines the posterior globe and functions to separate orbital fat from the sclera (Fig. 2-22). Just anterior to the equator of the eye, the four rectus muscles penetrate Tenon’s capsule and become surrounded by intra- and extraconal orbital fat. At this juncture, Tenon’s capsule unites with the capsule of the rectus muscle to form a muscle pulley or muscle sleeve (see Muscle Pulley, earlier). The muscle sleeve is an important surgical

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handbook of pediatric strabismus and amblyopia

Posterior Tenon's capsule Extraconal fat

Anterior Tenon's capsule

Muscle sleeve (pulley)

Conjunctiva Fused anterior Tenon's and conjunctiva

Intraconal fat Medial rectus muscle FIGURE 2-22. Drawing of a rectus muscle showing fascial relationships. Note that the muscle penetrates posterior Tenon’s capsule; the capsule at this point forms a muscle sleeve or muscle pulley. Intraconal and extraconal fat are isolated from the globe by Tenon’s capsule.

landmark when looking for a slipped or lost rectus muscle. A lost muscle is a rectus muscle that has become completely detached from the globe because of trauma or a surgical mistake.32,48 Once lost, the muscle will slip posteriorly within the muscle sleeve to be surrounded by intra- and extraorbital fat. To ﬁnd a lost muscle, ﬁrst ﬁnd the muscle sleeve located between the intraand extraconal fat; then, carefully follow the sleeve to retrieve the muscle. When looking for a lost medial rectus muscle, avoid the tendency to follow the sclera posteriorly, as this leads to the optic nerve. An important complication of attempted retrieval of a lost medial rectus muscle is inadvertent transection of the optic nerve that is enshrouded in postoperative scar tissue. Together, posterior Tenon’s capsule, anterior Tenon’s capsule, and the muscle sleeve are very important structures as they are the barrier that keeps orbital fat from the globe and extraocular muscles. If posterior Tenon’s capsule or muscle sleeve is traumatically or surgically violated, fat adherence can occur because orbital fat prolapses through the torn Tenon’s capsule and scars to the sclera or an extraocular muscle (Fig. 2-23). The scarring of orbital fat produces a restrictive scar, which extends from the periosteum to the eyeball. As the scar

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contracts over weeks to several months, the scar pulls the eye, producing a restrictive strabismus associated with limitation of eye movements. Fat adherence can occur as a complication of almost any extraocular surgery (e.g., strabismus surgery, retina surgery) or periocular trauma.31,49 Extreme care must be taken when operating in the area of orbital fat, which starts 10 mm posterior to the limbus. Once fat adherence occurs, it is almost impossible to correct. Surgically induced fat adherence can usually be avoided if the surgeon carefully dissects close to muscle belly or sclera, thus preserving the integrity of the overlying posterior Tenon’s capsule and muscle sleeve.

CHECK LIGAMENTS These are ﬁne falciform webs that overlie the rectus muscles and join the muscle capsule with overlying bulbar conjunctiva

A

B FIGURE 2-23A,B. Diagram modiﬁed after Parks and published in Ophthalmology by Wright (1986)49 shows the pathophysiology of the fat adherence syndrome. (A) Normal anatomy with orbital bone, periorbita, extraconal fat, muscle, and intermuscular septum. Note that the fat is isolated from muscle and sclera by intact Tenon’s capsule and intermuscular septum. (B) Violation of Tenon’s capsule with fat adherence to the globe and muscle (to right).

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at the muscle tendon (see Fig. 2-20). More posteriorly, check ligaments are probably the bands that connect the OL muscle ﬁbers to the surrounding muscle sleeve (muscle pulley). In the case of the superior and inferior rectus muscles, check ligaments also connect to the levator muscle and lower lid retractors, respectively. A recession or resection of vertical rectus muscles requires removal of these ligaments to avoid lid ﬁssure changes after surgery.

VASCULAR SUPPLY TO THE ANTERIOR SEGMENT The anterior segment and iris are supplied by the anterior ciliary arteries, conjunctival vessel, and the long posterior ciliary arteries (Fig. 2-24). Approximately 50% of the anterior segment circulation comes from the long posterior ciliary arteries and

FIGURE 2-24. Diagram of circulation of the anterior segment with the rectus muscle supplying the anterior ciliary arteries (aa); the deep long posterior arteries are also shown. (Figure published with permission of J.B. Lippincott Co. from Wright KW. Color Atlas of Ophthalmic Surgery: Strabismus. Philadelphia: Lippincott, 1991.47)

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50% from the anterior ciliary arteries. The conjunctival vessels also contribute to anterior segment circulation.14 Anterior ciliary arteries and the conjunctival vessels merge at the limbus to form the episcleral limbal plexus.27 These vessels in turn connect with the major arterial circle of the iris, which is also fed by the two long posterior ciliary arteries. The superior rectus, inferior rectus, and medial rectus muscles have at least two anterior ciliary arteries and are major contributors to the anterior segment circulation.18 The lateral rectus has a single anterior ciliary artery and, of the four recti muscles, the lateral rectus probably provides the least in the way of anterior segment circulation.20,41 The oblique muscles do not have anterior ciliary arteries, and they do not contribute to the anterior segment circulation. Iris angiograms can be used to assess anterior segment circulation in blue-eyed patients. Removal of a vertical rectus muscle will cause hypoperfusion in that area that relates to the vascular input.18 It is interesting that this hypoperfusion lasts only 1 to 2 months because its collateral circulation and vasodilatation will replenish the hypoperfused area.45 Additionally, infants and children do not typically show hypoperfusion even when multiple rectus muscles are removed. Removal of a rectus muscle during strabismus surgery will permanently interfere with vascular supply of the anterior ciliary arteries unless the surgery is performed speciﬁcally to maintain anterior segment circulation. Surgeries have been devised that attempt to maintain anterior segment circulation despite manipulations of the muscle position.24,45 Iris angiograms can be used to document anterior segment blood ﬂow from the anterior ciliary arteries in nonhuman primates. A muscle-to-sclera plication developed by this author (Wright plication) is designed to tighten a rectus muscle but spare the anterior ciliary arteries. Instead of resecting the muscle, as is done in the standard muscle tightening procedure, the Wright plication folds the muscle, suturing muscle to sclera without disrupting the anterior ciliary vessels. Figure 2-25 shows an iris angiogram after inferior rectus muscle plication and surgical removal of the other three rectus muscles in a nonhuman primate. The iris angiogram demonstrates intact perfusion from the inferior rectus muscle and hypoperfusion superiorly because the arteries of the other three rectus muscles had been sacriﬁced on surgical removal. Anterior segment ischemia can be a consequence of strabismus surgery, most often after a three- or four-muscle

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FIGURE 2-25. Monkey ﬂuorescein iris angiogram, early phase after Wright plication of the inferior rectus muscle and removal of the other three rectus muscles. Note the hypoperfusion superiorly (black area of iris) as the medial, lateral, and superior rectus muscles have been removed. The perfusion from the inferior rectus remains intact after the Wright plication because ﬂuorescence is seen inferiorly (white vessels on iris).46

transposition procedure.35,42 This is a rare occurrence, as collateral circulation from the long posterior ciliary arteries can usually maintain adequate perfusion to the anterior segment even when three or four rectus muscles have been removed.36 Factors that predispose to anterior segment ischemia include arteriosclerosis, hyperviscosity of the blood, and scleral encircling elements such as 360° retinal buckles posteriorly, all of which can compromise the long posterior ciliary arteries. Older patients have a higher likelihood for developing anterior segment ischemia, whereas infants and children are generally protected from this condition.15 Anterior segment ischemia has even been reported after removing as few as two rectus muscles in high-risk patients.12,15 It is important to remember, however, that disruption of anterior ciliary arteries associated with strabismus surgery is permanent, and anterior segment ischemia can occur years or decades later, as the collateral circulation diminishes with age.34

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PHYSIOLOGY OF OCULAR ROTATIONS Donder’s and Listing’s Laws Ocular movements are a result of contraction and relaxation of multiple muscle groups that act to rotate the eye around a ﬁxed center of rotation. There are three axes that pass through the center of rotation, termed the axes of Fick (Fig. 2-26). The axes of Fick include the Z axis (vertical orientation) for horizontal rotation, the X axis (horizontal orientation) for vertical rotation, and the Y axis (oriented with the visual axis) for torsional rotation. Listing’s plane is a vertical plane that includes the X, Z, and oblique axes that pass through the center of the eye (Fig. 2-26). Listing’s law states that virtually all positions of gaze can be achieved by rotations around axes that lie on Listing’s plane. Donder’s law is related to Listing’s law and states that there is a speciﬁc orientation of the retina and cornea for every position of gaze. This corneal orientation is speciﬁc for each position of gaze regardless of the path the eye took to achieve that position of gaze. Figure 2-27 demonstrates Listing’s and Donder’s laws, showing the speciﬁc corneal orientations for ocular rotations around various axes on Listing’s plane. Note that when rotations

B

A

C FIGURE 2-26A–C. The three axes of Fick allow horizontal rotation. (A) Vertical axis (Z axis): horizontal rotations. (B) Horizontal axis (X axis): vertical rotations. (C) Visual axis (Y axis): torsional rotations.

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FIGURE 2-27. Listing’s plane is shown in the center diagram, which includes the Z and X axes of Fick. Diagram shows that the eye can reach all positions of gaze by rotations around axes that are on Listing’s plane. In the center diagram, the O axes represent oblique axes that are on Listing’s plane and are oriented between the Z and X axes of Fick. Note that the oblique axes of rotation seen on the four corners of the diagram allow the eye to rotate obliquely, up and in, up and out, down and in, and down and out. Also, observe the pseudotorsion of the cornea when the eye rotates around the oblique axis.

are directly around the X axis (pure vertical movement) or directly around the Z axis (pure horizontal movement) there is no associated torsional rotation of the cornea. In contrast, oblique ocular rotations cause a torsional shift in the corneal orientation relative to the planar coordinates of Listing’s plane. This torsional shift relative to Listing’s plane is not due to true rotation around the Y axis and is therefore referred to as pseudotorsion. Active, or true, torsional rotations around the Y axis (cycloduction) are created by contraction of vertical and oblique muscles. True torsional movements normally occur to keep the eyes aligned during head tilting23 or occur pathologically when a vertical or an oblique muscle over- or underacts.21

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TABLE 2-2. Agonist–Antagonist Muscle Pairs. Medial rectus—Lateral rectus Superior rectus—Inferior rectus Superior oblique—Inferior oblique

Sherrington’s Law: Agonist and Antagonist Muscles As described in this chapter previously, ductions are monocular rotations and are clinically examined with one eye occluded to force ﬁxation to the eye being tested. Table 2-2 lists agonist– antagonist pairs for the primary function of the muscles. This relationship between agonist (contracting muscle) and antagonist (relaxing muscle) muscles is referred to as Sherrington’s law of reciprocal innervation. Sherrington’s law can be demonstrated by using electromyography (EMG). The EMG measures electrical potential changes within a muscle as the muscle ﬁbers contract and indicates the degree of overall neuromuscular activity. The EMG is performed by placing a needle electrode in the muscle (extracellularly) and then recording the ampliﬁed electrical activity from the muscle. Figure 2-28 shows results of EMG for agonist and antagonist muscles that demonstrates Sherrington’s law. The needle electrode is placed in the medial and lateral rectus muscles. At the beginning of the EMG tracing, there is lowamplitude tonic activity that maintains the eye position in

FIGURE 2-28. Sherrington’s Law: Electromyographic (EMG) tracing from the lateral rectus muscle (LR) and medial rectus muscle (MR). Note that when the eye adducts, the medial rectus muscle increases EMG activity as the muscle contracts. EMG activity from the lateral rectus muscle diminishes as the antagonist lateral relaxes.

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primary position. As the eye is adducted, the medial rectus contracts, resulting in increasing EMG activity, while the lateral rectus muscle simultaneously relaxes and EMG activity is inhibited. At the end of the tracing, both muscles show tonic activity to maintain eye position. In patients with motor neuron misdirection syndromes such as Duane’s retraction syndrome, Sherrington’s law is violated. In Duane’s syndrome, the lateral rectus muscle is innervated by a branch of the third nerve that also supplies the medial rectus muscle. When the patient adducts the eye, instead of the medial rectus contracting and the lateral rectus relaxing, both the medial and lateral rectus muscles contract simultaneously. It should be remembered that Sherrington’s law of reciprocal innervation refers strictly to monocular eye movements, as does the term ductions. A trick to remember this, is the S in Sherrington stands for Single eye.

Synergist The term synergist is used for muscles of the same eye that act to move the eye in the same direction. In other words, synergist muscles have common actions. For example, the superior oblique and the inferior rectus muscles both act as depressors; therefore, they are synergists for infraduction. These muscles are not, however, synergists for horizontal or torsional rotations, as the inferior rectus muscle is an adductor and extortor whereas the superior oblique muscle is an abductor and intortor. Table 2-3 lists synergist muscles for various duction movements. Note that synergist muscles relate to monocular rotations, not to be confused with yoke muscles involved with binocular eye movements (see Hering’s Law of Yoke Muscles, below). Like the S trick in Sherrington’s law, remember the S in Synergist stands for Single eye.

TABLE 2-3. Synergist Muscles. Duction

Primary mover

Secondary mover

Supraduction Infraduction Adduction Abduction Extorsion Intorsion

Superior rectus Inferior rectus Medial rectus Lateral rectus Inferior oblique Superior oblique

Inferior oblique Superior oblique Superior rectus/inferior rectus Superior oblique/inferior oblique Inferior rectus Superior rectus

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Oculomotor Reﬂexes Two important oculomotor reﬂexes are the vestibulo-ocular reﬂex (VOR) and optokinetic nystagmus (OKN). The vestibuloocular reﬂex functions to keep the eyes steady when the head moves. Vestibular stimulation, induced by turning the head, results in a compensatory movement of the eyes to maintain the position of gaze. If the head is rapidly turned to the left, the eyes move to the right with the same velocity. A similar reﬂex, the orthostatic reﬂex, is responsible for keeping the eyes torsionally aligned when the head is tilted. This reﬂex is the basis of the Bielschowsky head tilt test for vertical muscle palsies. Optokinetic nystagmus is a visually mediated reﬂex consisting of smooth pursuit alternating with saccadic reﬁxation as a series of objects cross the visual ﬁeld. The eyes follow a moving object with smooth pursuit, then use a saccadic movement in the opposite direction to reﬁxate on the next approaching target. The stimulus most commonly used to produce OKN is a pattern of black and white stripes presented on a rotating drum or moving tape. The best OKN stimulus ﬁlls the visual ﬁeld so there are no stationary objects for the subject to ﬁxate.

Hering’s Law of Yoke Muscles Normally, our two eyes move together in the same direction; this is termed a version movement. Coordinated binocular eye movements require symmetrical innervation of each eye. For example, when one looks to the left, the left lateral rectus and right medial rectus muscles simultaneously contract as the left medial and right lateral rectus muscles relax (Fig. 2-29). The paired agonist muscles from each eye are referred to as yoke muscles. In Figure 2-29, the left lateral and right medial rectus muscles are yoke agonist muscles whereas the left medial and right lateral are yoke antagonists. Hering’s law states that yoke muscles receive equal innervation. Remember, Hering’s law relates to yoke muscles and binocular eye movements (versions), whereas Sherrington’s law explains agonist–antagonist relationships and monocular eye movements (ductions). Figure 2-30 shows the yoke agonist muscles responsible for various ﬁelds of gaze. In most situations, the term yoke muscles refers to yoke agonist muscles.

FIGURE 2-29. Hering’s Law: Diagram of version movements to the left. As the left lateral rectus (LR) contracts (), the contralateral medial rectus (MR) simultaneously contracts (). Also note that the left medial rectus relaxes () and the right lateral rectus also relaxes ().

FIGURE 2-30. Yoke muscles are shown for speciﬁc ﬁeld of gaze. Top: gaze up and to the side with yoke muscles being the superior rectus (SR) and inferior oblique (IO) muscles. Middle: straight sidegaze with the yoke muscles being lateral rectus (LR) and medial rectus (MR). Bottom: gaze down and to the side with yoke muscles being the inferior rectus (IR) and superior oblique (SO).

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Versions Versions can be classiﬁed as follows: dextroversion for rightgaze, levoversion for leftgaze, supraversion for upgaze, and infraversion for downgaze. In contrast to ductions, versions are performed with both eyes open and compare how well the eyes move together in synchrony. Versions will identify a subtle restriction or paresis and muscle overaction that results in asymmetrical eye movements.

References 1. Atkinson J. Development of optokinetic nystagmus in the human infant and monkey infant: an analogue to the development in kitten. In: Freeman RD (ed) Developmental neurobiology of vision. New York: Plenum Press, 1979. 2. Bartini C, Horcholle-Bossavit G. Extraocular muscle afferents and visual input interactions in the superior colliculus of the cat. Prog Brain Res 1979;50:335. 3. Beisner DH. Reduction of ocular torque by medial rectus recession. Arch Ophthalmol 1971;85:13. 4. Bloom JN, Graviss ER, Mardelli PG. A magnetic resonance imaging study of the upshoot-downshoot phenomenon of Duane’s retraction syndrome. Am J Ophthalmol 1991;111:548–554. 5. Bremer DL, Rogers GL, Quick LD. Primary-position hypotropia after anterior transposition of the inferior oblique. Arch Ophthalmol 1986;104:229–232. 6. Clark RA, Miller JM, Demer JL. Three-dimensional location of human rectus pulleys by path inﬂections in secondary gaze positions. Investig Ophthalmol Vis Sci 2000;41:3787–3797. 7. Collins CC. The human oculomotor control system. In: Lennerstrand G, Bach–y-Rita P (eds) Basic mechanism of ocular motility and their clinical implications. New York: Pergamon, 1975:145–180 8. Cynader M, Berman N, Hein A. Recovery of function in cat visual cortex following prolonged deprivation. Exp Brain Res 1975;25:139– 156. 9. Daniel P. Spiral nerve endings in the extrinsic eye muscles of man. J Anat 1946;80:189. 10. Demer JL, Poulkens V, Miller JM, Micevych P. Innervation of extraocular pulley smooth muscle in monkeys and humans. Investig Ophthalmol Vis Sci 1997;38:1774–1785. 11. Demer JL, Oh SY, Poulkens V. Evidence for an active control of rectus extraocular muscle pulleys. Investig Ophthalmol Vis Sci 2000;41: 1280–1290. 12. Fells P, March RJ. Anterior segment ischemia following surgery on two rectus muscles. In: Reinecke RD (ed) Strabismus: proceedings of

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16.

17. 18. 19. 20. 21. 22. 23. 24.

25. 26.

27. 28.

29.

30. 31.

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the third meeting of the International Strabismological Association, May 10–12, 1978, Kyoto, Japan. New York: Grune & Stratton, 1978: 375–380. Fink WH. Surgery of the oblique muscles of the eye. St. Louis: Mosby, 1951:92–95. Fishman PH, Repka MX, et al. A primate model of anterior segment ischemia after strabismus surgery. Ophthalmology 1990;97(4):456–461. France TD, Simon JW. Anterior segment ischemia syndrome following muscle surgery. The AAPO&S experience. J Pediatr Ophthalmol Strabismus 1986;23:87–91. Guemes A, Wright KW. Effect of graded anterior transposition of the inferior oblique muscle on versions and vertical deviation in primary position. JAAPOS 1998;201–206. Hawes MJ, Dortzbach RK. The microscopic anatomy of the lower eyelid retractors. Arch Ophthalmol 1982;100(8):1313–1318. Hayreh SS, Scott WE. Fluorescein iris angiography. Arch Ophthalmol 1978;96:1390–1400. Helveston EM, Merriam WW, Ellis FD, et al. The trochlea: a study of the anatomy and physiology. Ophthalmology 1982;89:124–133. Hiatt RL. Production of anterior segment ischemia. Trans Am Ophthalmol Soc 1977;75:87–102. Jampel RS. The fundamental principle of the action of the oblique ocular muscles. Am J Ophthalmol 1970;69:623. Koornneef L. Orbital septa: anatomy and function. Ophthalmology 1979;86:876–880. Linwong M, Herman SJ. Cycloduction of the eyes with head tilt. Arch Ophthalmol 1971;85:570. McKeown CA, Lambert HM, et al. Preservation of the anterior ciliary vessels during extraocular muscle surgery. Ophthalmology 1989;96: 498–507. Mims JL, Wood RC. Bilateral anterior transposition of the inferior obliques. Arch Ophthalmol 1989;107:41–44. Mims JL, Wood RC. Anti-elevation syndrome after bilateral anterior transposition of the inferior oblique muscles: incidence and prevention. J Am Assoc Pediatr Ophthalmol Strabismus 1999;3(6):333–336. Morrison JC, van Buskirk EM. Anterior collateral circulation in the primate eye. Ophthalmology 1983;90:707–715. Oh SY, Poulkens V, Demer J. Quantitative analysis of rectus extraocular muscle layers in the monkey and humans. Investig Ophthalmol Vis Sci 2001;42(1):10–17. Parks MM, Bloom JN. The “slipped muscle.” In: Symposium on strabismus. Transactions of the New Orleans Academy of Ophthalmology. St. Louis: Mosby, 1978:1389–1396. Parks MM. Atlas of strabismus surgery. Philadelphia: Harper & Row, 1983. Parks MM. Causes of the adhesive syndrome. In: Symposium on strabismus. Transactions of the New Orleans Academy of Ophthalmology. St. Louis: Mosby, 1978:269–279.

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32. Plager DA, Parks MM. Recognition and repair of the “lost” rectus muscle. Ophthalmology 1990;97:131. 33. Porter JD, Baker RS, Ragusa RJ, Brueckner JK. Extraocular muscles: basic and clinical aspects of structure and functions. Surv Ophthalmol 1995;39:451–484. 34. Saunders RA, Sandall GS. Anterior segment ischemia syndrome following rectus muscle transposition. Am J Ophthalmol 1982;93: 34–38. 35. Saunders RA, Phillips MS. Anterior segment ischemia after three rectus muscle surgery. Ophthalmology 1988;95:533–537. 36. Simon JW, Price EC, et al. Anterior segment ischemia following strabismus surgery. J Pediatr Ophthalmol Strabismus 1984;21:179–184. 37. Spencer RF, Porter J. Structural organization of the extraocular muscles. In: Buttner-Ennever J (ed) Neuroanatomy of the oculomotor system. Amsterdam: Elsevier, 1988:33–79. 38. Stager DR, Weakley DR, Stager D. Anterior transposition of the inferior oblique: anatomic assessment of the neurovascular bundle. Arch Ophthalmol 1992;110:360–362. 39. Stager DR, Porter J, Weakley DR, Stidham DB. A comparative microscopic analysis of the capsule of the nerve to the inferior oblique muscle. Trans Am Ophthalmol Soc 1997;95:453–462; discussion 463–465. 40. Swan KC. Fascia in relation to extraocular muscle surgery. Arch Ophthalmol 1970;83:134–140. 41. Virdi PS, Hayreh SS. Normal ﬂuorescein iris angiographic pattern in subhuman primates. Investig Ophthalmol Vis Sci 1983;24:790–793. 42. von Noorden GK. Anterior segment ischemia following the Jensen procedure. Arch Ophthalmol 1976;94:845–847. 43. von Noorden GK. Letter to the Editor. A magnetic resonance imaging study of the upshoot downshoot phenomenon of Duane’s retraction syndrome. Am J Ophthalmol 1991;112:358–359. 44. Wilcox LM Jr, Keough EM, et al. The contribution of blood ﬂow by the anterior ciliary arteries to the anterior segment in the primate eye. Exp Eye Res 1980;30:167–174. 45. Wright KW, Lanier AB. Effect of a modiﬁed rectus tuck on anterior segment circulation in monkeys. J Pediatr Ophthalmol Strabismus 1991;28:77–81. 46. Wright KW, et al. Acquired inﬂammatory superior oblique tendon sheath syndrome: a clinicopathologic study. Arch Ophthalmol 1982; 100:1752–1754. 47. Wright KW. Color atlas of ophthalmic surgery: strabismus. Philadelphia: Lippincott, 1991. 48. Wright KW. Discussion of paper: Recognition and repair of the lost rectus muscle. Ophthalmology 1990;97:136. 49. Wright KW. The fat adherence syndrome and strabismus after retinal surgery. Ophthalmology 1986;93:411–415.

3 Binocular Vision and Introduction to Strabismus Kenneth W. Wright

I

n normal vision, both eyes are precisely aligned on an object of regard, so the images from that object fall on the fovea of each eye. Precise image orientation on corresponding retinal areas of each eye permits cortical processing, which results in the merging or fusion of the two images. This process is termed binocular fusion. There are two important aspects of binocular fusion: sensory fusion and motor fusion. This chapter discusses the process of binocular vision and provides an introduction to strabismus.

SENSORY FUSION Sensory fusion is the cortical process of blending the images from each eye into a single binocular stereoscopic image. This fusing occurs as optic nerve ﬁbers from the nasal retina cross in the chiasm to join the uncrossed temporal retinal nerve ﬁbers from the fellow eye. Together, ipsilateral temporal ﬁbers and contralateral nasal ﬁbers project to the lateral geniculate nucleus and then on to the striate cortex. This division of hemiﬁelds does not totally respect the midline. There is signiﬁcant overlap in the foveal area with some of the nasal foveal ﬁbers projecting to the ipsilateral cortex and some of the temporal foveal ﬁbers crossing to the contralateral cortex. Within the striate cortex, afferent pathways connect to binocular cortical cells that respond to stimulation of either eye. Retinal areas from each eye that project to the same cortical binocular cells are called corresponding retinal points. In Figure 3-1, points “A” left eye and “A” right eye, and points “B” left eye and “B” right eye, are cor70

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FIGURE 3-1. Vieth–Müller circle and the empirical horopter. By mathematical theorems, points on the Vieth–Müller circle should project to corresponding retinal points. Point A stimulates the nasal retina of the left eye and the temporal retina of the right eye, and these retinal areas should mathematically correspond. Psychophysical experiments, however, show that the retinal architecture does not follow the mathematical circle of Vieth–Müller and that points on the empirical horopter stimulate corresponding retinal points. The bottom of the ﬁgure shows the fusion of the images from each eye into a binocular perception.

responding retinal points. In humans, approximately 70% of the cells in the striate cortex are binocular cells whereas the minority are monocular cells. Binocular cortical cells, along with neurons in visual association areas of the brain, produce single binocular vision with stereoscopic vision.

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When a subject with normal eye alignment ﬁxes on a target, that target falls on both foveas. Mathematical theory predicts that objects peripheral to the ﬁxation target (points A and B in Fig. 3-1) will project to corresponding retinal points if the peripheral objects lie on a circle that passes through the optical centers of each eye. This mathematically determined circle of points is called the Vieth–Müller circle. As is often the case for mathematical explanations of biological phenomena, physiological experiments have shown that the Vieth–Müller mathematical model only partially works for visual perception. Psychophysical experiments indicate that the locus of points, which project to corresponding retinal points of each eye, is not a circle but actually takes the shape of an ellipse. This elliptical line of points, which project to corresponding retinal points, is the empirical horopter and is shown as a dotted line in Figure 3-1. Remember, the location of the horopter is determined by the point of ﬁxation. Objects located in front of or behind the empirical horopter will project to noncorresponding retinal points. In Figure 3-2A, note that point “A” is distal to the empirical horopter and stimulates binasal retina. Point “B” in Figure 3-2B, which is proximal to the horopter, stimulates bitemporal retina. These binasal and bitemporal retinal points are noncorresponding retinal points, and images falling on these points are termed disparate images. Disparate images have the potential for either producing stereoscopic vision or causing physiological diplopia.

Stereoscopic Vision The empirical horopter is a theoretical locus of points, and is inﬁnitely thin. All three-dimensional objects lie in front of and behind the horopter line; therefore, virtually all solid objects stimulate noncorresponding retinal points and result in disparate retina images. The brain, however, can merge or “fuse” images from slightly noncorresponding retinal points. This ﬁnite area in front of and behind the horopter line where objects stimulate noncorresponding retinal points, yet are still fusible into a single binocular image, is called Panum’s fusional area (Fig. 3-3). Stimulation of noncorresponding retinal points within Panum’s fusional area will produce three-dimensional vision. This ability for the brain to determine that images are falling on retinal points that are not exactly corresponding (i.e., disparate images) produces stereoscopic vision. Only horizontal retinal

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A

B FIGURE 3-2A,B. Empirical horopter and Panum’s fusional area. Objects that lie in front of or behind Panum’s fusional area will stimulate noncorresponding retinal points. (A) Patient ﬁxating on the star in the center of the empirical horopter. Point A, which is distal to the horopter, stimulates the binasal retinal points that are noncorresponding. (B) Patient ﬁxating on the same spot; however, point B is proximal to the Panum’s fusional area, and point B stimulates bitemporal retinal points that are noncorresponding. Point A in (A) would cause uncrossed diplopia, whereas point B in (B) would cause crossed diplopia. This type of diplopia is termed physiological diplopia.

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}

Empirical Horopter

Panum's fusional area

Stereoscopic Image

FIGURE 3-3. Diagrammatic representation of stereoscopic vision. Note that any three-dimensional objects will straddle the empirical horopter and parts of that object will be in front of or behind the empirical horopter; this stimulates noncorresponding retinal points that provide stereoscopic vision so long as the three-dimensional objects fall within Panum’s fusional area.

image disparities produce stereoscopic vision; vertical disparities do not. Panum’s fusional area is narrow at the center and gradually widens in the periphery reﬂecting the high resolution–small receptive ﬁelds in the central visual ﬁeld and low resolution–large receptive ﬁelds in the periphery. Large displacements are required for the peripheral retina to detect a change in receptive ﬁeld. Figure 3-3 shows a three-dimensional cube as a ﬁxation target. Note that the cube lies in front of and behind the empiri-

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cal horopter, projecting to noncorresponding retinal points. The fovea has high spatial resolution, so even small displacements off the horopter line (i.e., small image disparities) in the central visual ﬁeld are detected, resulting in ﬁne, high-grade stereoscopic vision. In contrast, as one moves to the peripheral ﬁelds, the receptive ﬁeld size enlarges and the spatial resolution decreases. The peripheral binocular visual ﬁelds are sensitive to large image disparities and provide coarse stereoacuity. This retinal architecture of high central resolution versus low peripheral resolution explains the excellent stereoacuity from central ﬁelds and progressively poorer stereoacuity from peripheral binocular retinal ﬁelds.

Physiological Diplopia If an object is too far off the horopter line and outside of Panum’s fusional area, then the images can no longer be fused and double vision may result (diplopia) (Figs. 3-2, 3-4). This type of double vision is a normal phenomenon and is termed physiological diplopia. Note that, in Figure 3-4, the pencil is in front of Panum’s fusional area and the pencil is, therefore, stimulating the temporal retinas of each eye. Because the temporal retina projects to the nasal visual ﬁeld (opposite ﬁeld), the observer perceives two pencils with the left image coming from the right eye and the right image coming from the left eye; this is called “crossed diplopia,” and occurs with bitemporal stimulation. Physiological diplopia would occur in everyday life; however, it is normally ignored or suppressed. You can experience physiological diplopia by simply ﬁxating on a distant object several feet away then placing a pencil a few inches from your nose. While you are looking at the distant object, the pencil will appear double. This is crossed diplopia: when you close your right eye the left pencil disappears, and when you close the left eye the right pencil disappears. You can demonstrate that Panum’s fusional area is narrow centrally and wide in the periphery by moving the pencil held at near to the right or left, while maintaining ﬁxation on a distance target. Observe that the physiological diplopia and image quality diminish when the pencil is moved into the peripheral binocular ﬁelds. (Remember to keep your ﬁxation on a distant object while the pencil is held at near.) Objects distal to Panum’s fusional area stimulate binasal retinal points and can cause uncrossed diplopia (see Fig. 3-2A). You can experience uncrossed diplopia by ﬁxating on a pencil a few

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FIGURE 3-4. A pencil is seen in front of Panum’s fusional area; this stimulates noncorresponding bitemporal retinal points. Because the temporal retina projects to the opposite ﬁeld (arrows), the patient perceives crossed physiological diplopia.

inches in front of you and observing that the distant objects are double (this may be difﬁcult to see).

Stereoacuity Testing Stereoscopic perception can be created from two-dimensional ﬁgures by presenting each eye with similar ﬁgures that are horizontally offset to produce bitemporal or binasal retinal image disparities. Bitemporal retinal stimulation within Panum’s fusional area gives the stereoscopic perception of an image coming toward the observer (Fig. 3-2B), and binasal retinal stimulation within Panum’s fusional area gives the perception of an image going away from the observer (Fig. 3-2A). Note that the upper circles in Figure 3-5 are displaced nasally. The displaced

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circles result in bitemporal retinal stimulation within Panum’s fusional area, and the circle will be perceived as a single circle coming up off the page. In contrast, temporal displacement of stereoscopic ﬁgures results in binasal retinal stimulation, with the perception of depth away from the observer and into the page. Most clinical stereoacuity tests present nasally displaced images to each eye by using mirror systems, red/green glasses

FIGURE 3-5. Diagrammatic representation of a contour stereogram. Polarized glasses donned by the patient match the orientation of two polarized plastic plates on the stereo book, so one eye sees one plate and the fellow eye sees the other plate. The polarization is oriented vertically over the left eye and horizontally over the right eye, so the left eye views the left ﬁgure with the upper circle shifted to the right, and the right eye views the right ﬁgure with the upper circle shifted to the left. This nasal displacement of the circles stimulates bitemporal disparate retinal points and produces the stereoscopic perception that the upper circle is raised off the page. Titmus testing uses nasally displaced ﬁgures to produce stereoscopic images that come up off the page, towards the observer.

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TABLE 3-1. Visual Acuity (VA) and Titmus Stereoacuity. Circles 9 8 7 6 5 4 3 2 1

40 s 20/25 50 s 20/30 60 s 20/40 80 s 20/50 100 s 20/60 140 s 20/70 200 s 20/80 400 s 20/100 800 s 20/200

Circles/seconds (s) of arc VA.4

with corresponding red/green ﬁgures, or polarized glasses with corresponding polarized ﬁgure plates (see Fig. 3-5). These systems provide different images to each eye separately under binocular viewing and are termed haploscopic devices. Stereoacuity can be quantiﬁed by measuring the amount of image disparity. The angle of disparity can be measured in seconds of arc. The minimum stereoscopic resolution is a disparity of approximately 30 to 40 s of arc. Stereoscopic resolution depends upon visual acuity, as poor vision in one or both eyes will decrease stereoacuity. A general guide on the effect of image blur on stereoacuity is seen in Table 3-1. Interpupillary distance also inﬂuences stereoacuity. The farther apart the two eyes, the greater the angle of visual disparity and the greater the stereoscopic potential. Additionally, the closer an object is to the eyes, the greater the angle of disparity; therefore, the better the stereoscopic view. As objects move away from the observer, the relative interpupillary distance diminishes as does the visual angle, so stereoscopic vision decreases for distance objects.

CONTOUR STEREOACUITY TEST Contour stereoacuity tests use stereoscopic ﬁgures with a continuous contoured edge (Fig. 3-5). The Titmus test is a popular contour stereoscopic test and measures disparities from 3000 s arc (the big ﬂy) to 40 s arc (ninth circle). Some pictures in the test are stereoscopic and others are ﬂat (two-dimensional). The patient is required to identify which ﬁgure is stereoscopic. Contour stereoscopic ﬁgures are clinically useful because the stereoscopic effect is obvious and easy to see, but they have the disadvantage of having monocular clues. Monocular clues allow patients who are stereoblind to identify the stereoscopic ﬁgures1,3; this occurs because each stereoscopic ﬁgure is made

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up of two drawings, nasally shifted off center (see Fig. 3-5). Patients with monocular vision can identify which ﬁgure is supposed to be stereoscopic, because that ﬁgure will be horizontally off center. Another type of monocular clue used by patients with alternating strabismus to falsely pass contour stereo tests is “image jump.”1 These patients alternate ﬁxation between the two horizontally displaced ﬁgures and identify the ﬁgure that jumps back and forth. Monocular clues work for stereoscopic ﬁgures with large disparities and if the stereoscopic ﬁgure is framed so the displaced ﬁgure looks off center. The ﬁrst three stereoscopic “circles” and ﬁrst stereoscopic “animal” on the Titmus stereoacuity test can often be identiﬁed by using monocular clues, but stereo ﬁgures with smaller disparities are difﬁcult to detect using monocular clues. One way to help verify that the patient has true stereoacuity is to retest with the Titmus test book turned 90° and see if the patient still sees the stereoscopic target. With the test book turned 90°, the targets are not stereoscopic, but the monocular clues still work. If the patient again identiﬁes the stereoscopic target, they are using monocular clues, not true stereopsis. For further veriﬁcation, turn the book 180° (upside down) and see if the patient notes that the stereo targets have returned but are now projecting in an opposite direction away from the patient. The Titmus “ﬂy” can be useful in preverbal children as young as 1 to 2 years of age. If a child startles to the ﬂy coming out of the page, then this is suggestive of gross stereopsis. Also, if a child clearly picks up the wings of the Titmus “ﬂy” well off the page, this is good evidence for at least some peripheral fusion.

RANDOM DOT STEREOACUITY TEST Random stereograms consist of two ﬁelds of randomly scattered dots or specks, with one ﬁeld of dots projected to each eye separately through a haploscopic device. Each ﬁeld of random dots is identical except for a group of dots that is displaced nasally. The group of displaced dots can take the form of any recognizable shape, such as the square shown in Figure 3-6. The nasally displaced square of dots stimulates bitemporal retinal points and produces the perception that a single square of dots is coming up off the page. Random dot stereoacuity tests have an advantage over contour stereo tests, as random dot tests have almost no monocular clues, and a positive response indicates true stereopsis with few false-positive responses.8 The problem with

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FIGURE 3-6. Diagrammatic representation of a Randot stereogram. The left eye sees one set of dots and the right eye sees a second set of dots. The dots are identical, except for the dots within the square that have been horizontally displaced (nasally in the ﬁgure). Nasal displacement stimulates bitemporal disparate retinal points and produces the stereoscopic perception that the square of circles is raised off the page. This clinical test for Randot stereoacuity consists of nasal displacement, so that the stereo images appear to come off the page.

random dot stereoacuity testing, however, is that many young, normal children and some normal adults have trouble seeing the random dot stereoscopic effect and falsely fail the test.

Monocular Depth Perception Depth perception can occur without stereoacuity. Monocular vision can provide information regarding depth and the distance of an object. Motion parallax, shadows, object overlap, and the relative size of objects give us monocular clues of depth. Motion

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parallax is the perception of a change in position of an object resulting from a change in position from where the object is viewed. For example, a monocular observer viewing a distant object will note that near objects move to the left as the observer moves his head to the right. Monocular clues can be so powerful that one-eyed patients, or patients with large-angle strabismus, can successfully perform a variety of tasks that require keen depth perception. Professional athletes, microsurgeons, even ophthalmologists have been successful using monocular depth perception.2

Bifoveal Fusion Marshall Parks coined the term “bifoveal fusion” or “biﬁxation” to indicate the normal state of binocular fusion.7 Bifoveal fusion includes high-grade stereoacuity of 40 to 50 s of arc, accurate eye alignment, and normal motor fusion. Patients with bifoveal fusion have normal retinal correspondence.

Rivalry Rivalry, or as it is sometimes termed, retinal rivalry, is a condition where a patient with normal binocular vision is presented with different images to corresponding retinal points of each eye. Instead of seeing two different images superimposed on each other (termed “confusion”), the subject perceives patchy dropout of each image where the images binocularly overlap. Rivalry can be demonstrated most dramatically by presenting parallel lines to each eye with the lines rotated 90° in one eye (Fig. 3-7). The observer will perceive that some of the lines disappear in a spotty fashion as they cross over each other. You can experience rivalry by placing a pencil horizontally 2 inches in front of one eye and your index ﬁnger vertically 2 inches in front of the other eye. Note that there is patchy dropout of either the pencil or the index ﬁnger where they overlap. The rivalry phenomenon is often described as retinal rivalry; however, it is a complex interaction involving cortical inhibition. The presence of rivalry indicates the existence of bifoveal fusion potential.

Motor Fusion Motor fusion is the mechanism that allows ﬁne-tuning of eye position to maintain eye alignment. It acts as a locking mecha-

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A

C B FIGURE 3-7A–C. Diagonal lines are presented to each eye with the lines oriented 90° to each other (A,B). The combined binocular perception is a patchy pattern, with lines from each eye being seen; however, because of rivalry, crossing lines are not seen (C).

nism to keep the eyes aligned on visual targets as they move through space. Motor fusion also controls innate tendencies for the eyes to drift off target. These correctional eye movements that maintain binocular foveal alignment provided by motor fusion are termed fusional vergence movements. Unlike version movements, in which both eyes move in the same direction, vergence eye movements are in the opposite direction; they are termed “disjunctive” and disobey Hering’s law. Convergence, for example, is invoked when one eye follows an object moving from distance to near and results in both eyes moving to the midline with the right eye moving left and the left eye moving right (Fig. 3-8A). You can experience convergence by ﬁxating on a pencil at arm’s length and slowly bringing the pencil to your nose. As the pencil approaches your nose, the eyes converge to hold alignment on the pencil. Convergence movements are the strongest vergence

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movements, and there are several mechanisms that contribute to convergence (see Vergence Amplitudes, following). In addition to convergence, there are two other vergence movements: divergence and vertical vergence (Fig. 3-8B,C). Divergence is used to follow an object moving away and consists of the right eye moving right and left eye moving left. Vertical vergence is the weakest vergence movement and keeps our eyes from drifting vertically. Vertical vergence is depression of one eye with elevation of the fellow eye. Measurement of vergence amplitudes and a discussion of the various mechanisms of convergence are presented next.

A

B

C FIGURE 3-8A–C. Vergence. (A) Convergence of the eyes as the pencil approaches from the distance. (B) Divergence as the patient changes ﬁxation from a near target to a distance target. (C) Vertical vergence, as the patient vertically aligns the eyes to compensate for the vertical phoria or an induced deviation produced by a vertical prism.

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INTRODUCTION TO STRABISMUS Normally our eyes are well aligned so the foveas are aimed on the same visual target; this is termed orthotropia (Fig. 3-9). Strabismus is the term for ocular misalignment, or if there is an underlying tendency toward misalignment. Another term for strabismus is “squint.” This term comes from the fact that strabismic patients often squint one eye to block out one of the two images that they see. A manifest misalignment is called a heterotropia or tropia for short. A tropia causes double vision (diplopia) if acquired after 7 to 9 years of age; however, children under 6 to 7 years of age will cortically suppress vision from the deviated eye. Cortical suppression is a neurological mechanism that allows children to eliminate diplopia. Children who alternate ﬁxation between eyes (i.e., alternate suppression) will retain equal vision, but constant suppression of the deviated eye can cause decreased vision of the deviated eye, resulting in strabismic amblyopia. In contrast, a hidden tendency for an eye to drift is termed heterophoria or phoria. Patients with a phoria have a latent tropia and use motor fusion to maintain proper alignment. One can demonstrate the latent deviation of a phoria by disrupting binocular fusion. Occluding or fogging the vision of one eye (either eye) will disrupt fusion, and the eye behind the occluder will deviate (Fig. 3-10). Identifying a phoria indicates that some degree of motor fusion is present. Orthophoria is the state of the eyes where there is no strabismus and not even a tendency for the eyes to drift (i.e., no phoria). Orthophoria is rare to non-

FIGURE 3-9. Normal eye alignment with image falling on both foveas.

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A

B FIGURE 3-10A,B. Alternate cover test in patient with an esophoria. (A) Eyes are straight; the patient has a tendency to cross (esophoria), but fusional divergence maintains proper alignment. (B) Left eye is covered, dissociating fusion and allowing the left eye to manifest the esophoria. Note that the left eye turns in under the cover.

existent, as virtually all normally sighted people, with normal bifoveal fusion, have a small phoria but maintain alignment through motor fusion. Thus, most normal people are orthotropic but heterophoric. Phorias may spontaneously become manifest under conditions such as fatigue or illness that can cause central nervous system depression and diminish motor fusion. Central nervous system depressants also diminish motor fusion, and a patient with a large phoria may manifest their deviation after imbibing alcoholic beverages or taking sedatives. (This explains why the cowboy sees double after celebrating in town with one too many whiskies.) A large phoria that is difﬁcult to control may spontaneously become manifest, and this is called an intermittent tropia. Strabismus most commonly occurs in infancy or childhood and is usually idiopathic or related to a refractive error. In most of these cases, the eye muscles are normal and the eye can rotate freely. Less often, mechanical restriction of eye movements (restrictive strabismus) or an extraocular muscle paresis (paralytic strabismus) causes the strabismus. A blind eye may also drift, and this is termed sensory strabismus.

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Ocular misalignment may be horizontal, vertical, torsional, or any combination of these. Strabismus is described by preﬁxes that tell the direction of the deviation: eso, turning in; exo, turning out; and hyper, vertical deviation. A sufﬁx is added to the preﬁx to denote if the strabismus is a tropia or phoria. An esodeviation that is a tropia is termed an esotropia (ET) and a phoria is termed an esophoria (E); likewise, an exodeviation is either an exotropia (XT) or exophoria (X). The strabismic patient will have one eye ﬁxing on a target and the fellow eye will deviate. With esotropia, the deviated eye turns in so the target image falls nasal to the fovea (Fig. 3-11). In exotropia, the eye

FIGURE 3-11. Alternating esotropia. Top diagram: right eye is ﬁxing and the image is aligned with the right fovea while the image falls nasal to the left fovea as the left eye is deviated. Bottom diagram: left eye is ﬁxing with the image falling on the left fovea and the image falling nasal to the right fovea as the right eye is deviated.

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FIGURE 3-12. Alternating exotropia. Top diagram: right eye is ﬁxing with the left eye and the image falling temporal to the fovea. Bottom diagram: exotropic left eye is ﬁxing with a right exotropia and the image falling temporal to the right fovea.

turns out and the target image is temporal to the fovea (Fig. 312). Note that ﬁxation can switch from eye to eye. According to Hering’s law, as the deviated eye moves into primary position, the ﬁxing eye turns in the same direction to become the deviated eye (compare upper and lower drawings of Figs. 3-11 and 3-12). Vertical strabismus can be categorized as hypertropia or hypotropia. Because of Hering’s law, a left hypertropia is the same deviation as a right hypotropia, depending on which eye is ﬁxing (Fig. 3-13). In contrast to a horizontal deviation, when

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FIGURE 3-13. Alternating left hypertropia. Top left: right eye ﬁxing and a left hypertropia. Top right: retinal image (x) is falling on the fovea (small dot) of the right eye; however, the left fovea is rotated down (left hypertropia) so the retinal image (x) is located above the fovea (small dot). Bottom: left eye ﬁxing with right eye turned down. Now the retinal image (x) falls below the right fovea, which is rotated up (right hypotropia).

describing a hyperdeviation we must identify which side the hypertropia is on, either right hypertropia (RHT) or left hypertropia (LHT). By convention, we usually refer to a vertical deviation as a hypertropia, rather than use the term hypotropia, unless there is an obvious restriction or paresis that keeps one eye in a hypotropic position. This convention has practical importance as it minimizes confusion over which terminology is used, thus reducing the risk of inadvertently operating for a right hypotropia when the patient actually had a right hypertropia. Cyclotropia, or torsion, refers to a twisting misalignment around the Y axis of Fick. Excyclotropia (extorsion) is a temporal rotation of the 12 o’clock position, whereas incyclotropia (intorsion) means a nasal rotation of the 12 o’clock position. Normally the fovea should be aligned between the middle and the lower pole of the optic disc (Fig. 3-14, top). If the fovea is below the lower pole of the optic disc by direct view (above the disc in the indirect ophthalmoscopic view), this indicates objective extorsion (Fig. 3-14, bottom left). A fovea oriented above the middle of the optic disc by direct view (below the middle in the indirect ophthalmoscopic view) indicates intorsion (Fig. 3-14, bottom right). Torsion can also be measured by the Maddox rod test, and this is termed subjective torsion. Torsional motor

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fusion is weak to nonexistent; therefore, a tendency for torsional misalignment is manifest as a tropia and, for practical purposes, torsional phorias do not exist. There are consequently no torsional vergence eye movements. A small amount of torsional misalignment, however, is tolerated surprisingly well as the brain will accept up to 5° of torsional misalignment. Patients with a tropia less than 10 prism diopters (PD) will often have peripheral fusion and have a phoria coexisting with a small tropia. This condition is called the monoﬁxation syndrome and is associated with peripheral binocular fusion, central ﬁxation with the preferred eye, and central suppression of the foveal area in the fellow eye. Tropias greater than 10 PD preclude fusion, as the disparity of the images is too great to allow for even peripheral fusion. Patients with a tropia greater than 10 PD will not have motor fusion and will not have a coexisting phoria.

FIGURE 3-14. Ocular torsions through the direct view (left eye). Top: normal fovea to disc relationship with the fovea located along the lower half of the disc. Lower left: extorsion with the fovea below the lower half of the disc. Lower right: intorsion with the fovea above the lower half of the disc. In actuality, it is the disc that rotates around the fovea.

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Prisms and Strabismus Prisms are important tools for the diagnosis and treatment of strabismus, as they are used to measure and neutralize ocular deviations. A prism bends light toward the base of the prism (Fig. 3-15) because light has both particle and wave characteristics. As light passes through the prism, the part of the light wave closest to the prism base has more prism to traverse than the part of the wave closest to the apex. This is analogous to a row of soldiers marching through a triangle of sand; the soldiers walk slowly through sand so those at the base of the triangle exit the sand after the soldiers at the apex. The direction of the marching soldiers turns toward the base of the triangle as they exit. The ability of a prism to bend light is measured in prism diopters (PD). Light travels slower through the plastic prism than it does through air, so light toward the base of the prism takes longer to exit than light traversing the apex. The exit time differential causes the light to bend toward the base of the prism. One prism diopter will shift light 1 centimeter (cm) at 1 meter (m) or a displacement of approximately 0.5°. A 20 PD esotropia

A B C FIGURE 3-15A–C. Diagram of the effect of a prism over one eye. (A) Patient ﬁxates on the X. (B) A prism is introduced, and the image is displaced toward the base of the prism and off the fovea. Note that the patient will perceive the image to jump in the opposite direction. Thus, a patient will perceive the image to jump in the direction of the apex of the prism. (C) Patient reﬁxates to place the image on the fovea by rotating the eye toward the apex of the prism. Note that when a prism is introduced, the patient will always reﬁxate by rotating the eye in the direction of the apex of the prism.

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would mean the eye turns in approximately 10°. When a prism is placed in front of one eye, it moves the image off the fovea, causing a perceived image “jump.” The retinal image will shift toward the base of the prism, but the perceived image jump is in the opposite direction, toward the apex of the prism; this is because the retinal images are reversed, right/left and up/down (Fig. 3-15A,B). To reﬁxate on the shifted image, the eye will move in the direction of the prism’s apex, thus aligning the fovea with the new image location (Fig. 3-15C).

Prism Neutralization of a Deviation Prisms can be used to optically neutralize or correct strabismus. A prism acts to change the direction of the incoming image so the retinal image in each eye falls directly on the fovea. Neutralization occurs when enough prism is placed in front of the eye so the two foveas are aligned on the same object of regard. For example, when a base-out prism (prism held horizontally with the apex directed toward the nose) is placed in front of the deviated eye of a patient with esotropia, the retinal image shifts temporally toward the fovea (Fig. 3-16). If the correct amount of prism is used, the retinal image will fall directly on the fovea of the deviated eye. Thus, as seen in Figure 3-16B, the deviation has been optically neutralized by the prism even though the eye is still anatomically deviated. The rule for neutralizing a deviation is to orient the prism so the apex is in the direction of the deviation. For esotropia, the apex is directed nasally and, for exotropia, the apex is directed temporally. The apex is directed superiorly over a hypertropic eye and inferiorly over a hypotropic eye. The prism can also be placed in front of the ﬁxing eye (straight eye) to neutralize the deviation. If the prism is placed base-out in front of the ﬁxing eye (Fig. 3-17), the retinal image will move temporal to the fovea (Fig. 3-17A,B). The ﬁxing eye will see the image shift and will immediately rotate nasally to reestablish foveal ﬁxation (Fig. 3-17). As the ﬁxing eye rotates nasally, the deviated eye rotates temporally causing a version movement to the right (Fig. 3-17B). Therefore, when a base-out prism is placed in front of the ﬁxing eye, both eyes move in the same direction as the apex of the prism, and both foveas shift into alignment (Fig. 3-17B,C). In Figure 3-17C, both eyes have shifted to the right, with the left eye now turned in nasally and the right eye now straight in primary position. The previously

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A

B FIGURE 3-16A,B. Prism neutralization. (A) Patient with an esotropia. (B) A prism is introduced to direct the image onto the fovea of the left eye, thus correcting, or neutralizing, the deviation.

deviated right eye is now straight and in alignment with the ﬁxation target. Thus, one can place a prism in front of either eye or even split the prisms between the eyes to neutralize a strabismic deviation.

Prism-Induced Strabismus A prism placed over one eye in a patient with straight eyes will induce a deviation and produce strabismus. A base-in prism induces esotropia, as the target image is displaced nasal to the fovea (Fig. 3-18). Likewise, a base-up prism induces a hypertropia and a base-out prism induces an exotropia.

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A

B

C FIGURE 3-17A–C. Neutralization of an esotropia by placing the prism in front of the ﬁxing eye. (A) Esotropia with left eye ﬁxing. (B) Prism is placed base out in front of the ﬁxing eye (left eye), which displaces the image temporally off the fovea. The left eye rotates nasally to reﬁxate to the displaced image. As stated by Hering’s law, both eyes rotate in the direction of the apex of the prism. (C) Patient ﬁxing through the prism, left eye. The left eye has deviated nasally to put the image on the fovea. The right eye has moved temporally and is also in alignment with the ﬁxation target.

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A

B

C FIGURE 3-18A–C. Prism-induced esotropia. Patient with straight eyes and binocular vision is given an esotropia by placing a base-in prism over one eye. (A) Patient orthotropic with images falling on both foveas. (B) Base-in prism is placed before the left eye causing the image to move nasally off the fovea. Patient is ﬁxing with right eye. (C) Patient now ﬁxates with the left eye, viewing through the base-in prism. Left eye moves temporally to place the image on the fovea and, because of Hering’s law, the right eye moves nasally to displace the right retinal image nasally off the fovea.

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Prism-Induced Vergence Normal adult subjects with binocular fusion will see double when a prism is placed in front of one eye. If the prism is relatively small, the patient’s fusional vergence eye movements will be able to realign the eyes to keep the images appropriately placed on the foveas. The prism will initially invoke diplopia and the patient will realign the eyes within a second or two to replace the diplopia with single binocular vision. A base-out prism evokes fusional convergence, a base-in prism causes fusional divergence, and a base-up or base-down prism will evoke fusional vertical vergence. Figure 3-19 shows the steps of prism-induced convergence. A base-out prism placed over one eye will displace the retinal image off the fovea onto temporal retina, inducing an exotropia (Fig. 3-19A,B). The eye behind the prism moves nasally to reﬁxate to the fovea and the fellow eye moves temporally in a version movement (Hering’s law) (Fig. 319B). Diplopia occurs brieﬂy until fusional convergence is used to realign the eyes so retinal images can fall directly on each fovea (Fig. 3-19C,D). The key aspect of the convergence movement is the nasal fusional movement of the eye without the prism (Fig. 3-19C). Note that, after prism-induced strabismus in a patient with fusion, a compensatory vergence movement will occur in the eye without the prism (Fig. 3-19C). Prism-induced strabismus in a patient without fusion results in a version movement of both eyes without a subsequent vergence movement (see Fig. 3-18C).

Fusional Vergence Amplitudes Vergence movements compensate for phorias and keep the eyes aligned as targets move in depth throughout space. A patient with an exophoria uses convergence; those with esophorias use divergence, and hypertropias are controlled with vertical vergence. Convergence is by far the strongest of the vergence movements and can be strengthened by eye exercises if convergence is ineffective. Divergence is relatively weak and does not signiﬁcantly improve with eye exercises. The strength of vergence movements can be measured in prism diopters and is called fusional vergence amplitudes. Fusional vergence amplitudes are measured by inducing a deviation to stimulate a motor fusion to correct the induced deviation. Induce an exodeviation to test convergence (base-out

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A

B FIGURE 3-19A–B. Four steps of prism convergence. (A) Eyes are well aligned in a patient with good fusional convergence. (B) Exophoria is created by introducing a base-out prism in front of the left eye. Patient initially ﬁxates with the left eye, causing a version movement to the right, thus placing the left fovea on the image.

prism), an esodeviation for divergence (base-in prism), and a hyperdeviation for vertical vergence. Start by inducing a small deviation that can be fused and gradually increase the deviation until vision is blurred (blur point), then increase until fusion breaks (break point). A deviation can be induced by placing prisms (usually in the form of a prism bar) over one eye or by

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C

D FIGURE 3-19C–D. (C) Because of Hering’s law, the right eye also rotates and the image is now off the right fovea. To compensate for this, patient exercises fusional convergence and the right eye rotates nasally to put the image on the fovea; this is a vergence movement in distinction to the version movement seen in (B). (D) Patient is once again fusing, using fusional convergence to maintain eye alignment on the ﬁxation target. Note that the eye behind the prism is deviated nasally. The base-out prism actually induces an exophoria, even though the eye behind the prism is nasally deviated and looks esotropic.

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TABLE 3-2. Normal Fusion Vergence Amplitudes.

Convergence Divergence Vertical vergence

Distance (6 m)

Near (1/3 m)

20–25 PD 6–8 PD 2–3 PD

30–35 PD 8–10 PD 2–3 PD

PD, prism diopter.

moving the amblyoscope arms off parallel. Measure nearconvergence amplitudes by placing a base-out prism bar over one eye, starting with 4 PD, having the patient ﬁxate on an accommodative target at a distance of 33 cm. Then, move the bar up slowly to increase the base-out prism. The eye behind the prism bar will progressively turn in to converge as the prism is increased. The greatest prism that the patient can fuse is the fusional vergence amplitude. Prisms larger than this will break fusion and one eye will turn out, usually causing diplopia. Have the patient note when the ﬁxation target blurs (i.e., blur point), and when it becomes double (i.e., break point). Table 3-2 shows normal fusion vergence amplitudes based on the break point. The maximum base-out prism that can be fused is around 30 PD (convergence), the maximum base-in prism that can be fused is 6 to 10 PD (divergence), and the maximal vertical prism that can be fused is usually 2 to 3 PD (vertical vergence). In certain conditions, divergence and vertical vergence fusional amplitudes can be quite large. Patients with congenital superior oblique palsy, for example, can have vertical fusion vergence amplitudes up to 25 to 30 PD.

Types of Convergence There are various mechanisms of convergence; these include fusional convergence, accommodative convergence, tonic convergence, voluntary convergence, and proximal or instrument convergence.

FUSIONAL CONVERGENCE Fusional convergence is based on binocular vision. Occluding, or severely blurring the image of one eye, will disrupt fusional convergence; however, convergence mechanisms still function when binocular vision is suspended.

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ACCOMMODATIVE CONVERGENCE AND THE NEAR REFLEX When an object approaches from distance to near, the images falling on the retina are displaced temporally, then blur and enlarge. These retinal image changes stimulate the near reﬂex. The near reﬂex includes accommodation, convergence, and pupillary miosis. The ciliary muscles contract to increase the lens curvature and focus the image (accommodation). Contraction of both medial rectus muscles occurs to keep the eyes aligned on target (convergence), and the pupil constricts to increase the depth of focus. The synkinetic reﬂex of accommodation and convergence is termed accommodative convergence. Accommodation is one of the main drivers of convergence. For any individual, a speciﬁc amount of accommodation will result in a speciﬁc amount of convergence. The quantitative relationship between the amount of convergence associated with an amount of accommodation is referred to as the AC/A ratio (accommodative convergence/accommodation). A high AC/A ratio indicates overconvergence whereas a low AC/A ratio indicates convergence insufﬁciency. Patients with a high AC/A ratio are predisposed to developing esotropia (crossed eyes) at near, and a low AC/A ratio causes an exotropia (eye turning out) at near. The normal AC/A ratio is between 4 and 6 PD of convergence for every diopter of accommodation. Patients with wide interpupillary distances (PD) will have to have a relatively high AC/A ratio to converge sufﬁciently and keep both eyes aligned on near targets. The methods for measuring the AC/A ratio are described in Chapter 5.

TONIC FUSIONAL CONVERGENCE Tonic fusional convergence is a type of fusional convergence that persists even after monocular occlusion is introduced; this is a form of proprioceptive eye position control, which keeps the eyes converging even after one eye is occluded. Tonic fusional convergence dissipates with prolonged monocular occlusion. Patching one eye for 30 to 60 min eliminates most tonic fusional convergence. Tonic fusional convergence is referred to as tenacious proximal fusion by Kushner.5

VOLUNTARY CONVERGENCE Voluntary convergence is voluntarily invoked. Comedians use this to cross their eyes, and patients will voluntarily converge to produce convergence nystagmus.

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PROXIMAL OR INSTRUMENT CONVERGENCE This type of convergence is induced by a psychological awareness of an object at near, or when one views an object through an instrument such as a microscope.

Comitant Versus Incomitant Strabismus Strabismus can be classiﬁed into two broad categories: comitant and incomitant. Comitant strabismus is when the deviation measures the same in all ﬁelds of gaze. Most types of congenital and childhood strabismus are comitant. With comitant strabismus, both eyes move together equally well and there is no signiﬁcant restriction or paresis. Comitant strabismus is usually a “good” sign and indicates that the strabismus is not secondary to a neurological problem. Occasionally, however, acquired neurological disease processes, such as early-onset myasthenia gravis, chronic progressive external ophthalmoplegia (CPEO), or even a mild bilateral sixth nerve palsy, can initially present as a clinically comitant strabismus. Incomitant strabismus means the deviation is different in different ﬁelds of gaze. In the vast majority of cases, incomitance is caused by a limitation of ocular rotations secondary to ocular restriction or extraocular muscle paresis. Causes of ocular restriction include a tight or stiff muscle and periocular adhesions to the eye. Muscle paresis can be caused by a lack of innervation (i.e., third, sixth, or fourth nerve paresis), traumatic muscle damage, an overrecessed or lost muscle, or neuromuscular junction disease such as myasthenia gravis. Figure 3-20 shows an example of an incomitant esotropia secondary to limited abduction of the left eye. When the patient in Figure 3-20 looks to the left, the left eye cannot fully abduct; thus, the right eye overshoots and creates an esotropia (ET) that increases in leftgaze (Hering’s law of yoke muscles). In this example, the limited abduction could be due to either restriction (e.g., a tight left medial rectus muscle or a nasal fat adherence scar to the globe) or paresis (e.g., left sixth nerve palsy or left slipped lateral rectus muscle). Methods for diagnosing restriction and paresis are presented in Chapter 5.

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FIGURE 3-20. Left lateral rectus paresis. In primary position, there is a moderate esotropia. In right gaze, the esotropia (ET) diminishes, and in left gaze the esotropia increases. A tight left medial rectus muscle would give the same pattern of incomitance.

Primary Versus Secondary Deviation Patients with incomitant strabismus secondary to ocular restriction or muscle paresis will show a larger deviation when the eye with limited ductions is ﬁxing (secondary deviation) than when the eye with full ductions ﬁxates (primary deviation); this is in accord with Hering’s law. As shown in Figure 3-21, the primary deviation is small because relatively little innervation (1) is needed to keep the eye in primary position when the nonparetic

A B FIGURE 3-21A,B. Left sixth nerve palsy. (A) Normal right eye ﬁxating with little effort. Only 1 innervation is needed to put the eye on target; there is a small esotropia of 25 PD. (B) Change of ﬁxation to the left eye. Because the left lateral rectus muscle is weak, it requires 4 innervation to bring the left eye to primary position to view the target. The right medial rectus muscle is the yoke muscle to the weak left lateral rectus muscle, so the right medial rectus muscle also gets 4 innervation. The 4 innervation of the normal right medial rectus results in a large esotropia of 50 PD.

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right eye is ﬁxing (Fig. 3-21A). The paretic eye receives the same 1 innervation and turns in slightly because the left lateral rectus muscle is slightly weaker than its antagonist, the left medial rectus muscle. The secondary deviation is larger because the weak left lateral rectus muscle must receive a tremendous amount of innervation (4) to bring the left eye into primary position when the paretic eye ﬁxates (Fig. 3-21B). Both the paretic left lateral rectus and its yoke muscle, the right medial rectus, receive 4 innervation because of Hering’s law. This excess drive to the healthy right medial rectus muscle causes a large secondary nasal deviation of the right eye. This same mechanism of primary and secondary deviations also applies to restrictions. Primary overaction of oblique muscles can also cause incomitance. What we clinically refer to as primary muscle overaction, however, may actually represent a previous paresis of the antagonist and secondary overaction of the agonist muscle.

References 1. Archer SM. Stereotest artifacts and the strabismus patient. Arch Clin Exp Ophthalmol 1988;226:313–316. 2. Burden AL. The stigma of strabismus. Arch Ophthalmol 1994;112: 302. 3. Clarke WN, Noel LP. Stereoacuity testing in the monoﬁxation syndrome. J Pediatr Ophthalmol Strabismus 1990;27:161–163. 4. Donzis PB, et al. Effect of binocular variations of Snellen’s visual acuity on Titmus stereoacuity. Arch Ophthalmol 1983;101:930–932. 5. Kushner BJ. Exotropic deviations: a functional classiﬁcation and approach to treatment. Am Orthopt J 1988;38:81–93. 6. Levy NS, Glick EB. Stereoscopic perception and Snellen visual acuity. Am J Ophthalmol 1974;78:722–724. 7. Parks MM. The monoﬁxation syndrome. Trans Am Ophthalmol Soc 1969;12(42):1246. 8. Reincke RD, Simons K. A new stereoscopic test for amblyopia screening. Am J Ophthalmol 1974;78:714–721.

4 Visual Development and Amblyopia Kenneth W. Wright

NORMAL VISUAL DEVELOPMENT Monocular Visual Development At birth, visual acuity is poor, in the range of hand motions to count ﬁngers. For the most part, this is due to immaturity of visual centers in the brain responsible for vision processing. Visual acuity rapidly improves during the ﬁrst few months of life as clear in-focus retinal images stimulate neurodevelopment of visual centers, including the lateral geniculate nucleus and striate cortex.52 Dropout and growth of neuronal connections give rise to the organizational reﬁnement and establish highresolution receptive ﬁelds corresponding to the central foveal area.18,23 Normal visual development requires appropriate visual stimulation, including clear retinal images, with equal image clarity in both eyes (Table 4-1). Visual development is most active and vulnerable during the ﬁrst 3 months of life, which is termed the critical period of visual development.13 Figure 4-1 shows a curve of visual acuity improvement versus age. Note the curve is steepest during the ﬁrst months of life, relative to the critical period of visual development. Visual acuity development continues up to 7 to 8 years of age, but development is slower and plasticity is progressively less in later childhood. Abnormal visual stimulation by a blurred retinal image or strabismus during early visual development (e.g., congenital cataract, strabismus) can result in permanent damage to visual centers in the brain (see section on amblyopia later in this chapter). Early treatment of pediatric eye disorders is important to promote normal visual development. 103

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TABLE 4-1. Requirements for Normal Visual Development. Clear retinal images Equal image clarity Proper eye alignment

Binocular Visual Development Binocular visual development occurs in concert with improving monocular vision.7 Basic neuroanatomy tells us that the two eyes are linked, as nasal retinal axons cross to meet temporal retinal axons in the chiasm, then proceed to join neurons in the lateral geniculate nucleus. Neurons in the lateral geniculate nucleus project to the striate cortex to connect with binocular cortical neurons that respond to stimulation of either eye and monocular cortical neurons that respond to the stimulation of only one eye. In humans, and in most animals with binocular vision, approximately 70% of the neurons in the striate cortex are binocular neurons whereas the minority are monocular. Binocular cortical neurons along with neurons in visual association areas of the brain produce binocular stereoscopic vision. Animal studies demonstrate that binocular cortical neurons are present from birth.37,57 Maintenance and reﬁnement of these binocular neuroanatomic connections and the development of normal binocular visual function, however, are dependent on

FIGURE 4-1. Curve represents visual acuity development with age on the horizontal axis and Snellen acuity on the vertical axis. Note the exponential improvement in visual acuity during the critical period of visual development (birth to 3 months). m, months; y, years.

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appropriate binocular visual stimulation. Requirements for normal binocular visual development include clear and equal retinal stimulation and proper eye alignment (see Table 4-1). Binocular vision and fusion have been found to be present between 1.5 and 2 months of age,4,26 while stereopsis develops later, between 3 and 6 months of age.2,3,17 This author cared for a patient with a transient congenital sixth nerve palsy who presented at 3 weeks of age with a compensatory face turn to obtain binocular fusion. This single case suggests that early motor fusion may be present as early as 3 weeks of age.

NEONATAL ALIGNMENT Eye alignment is variable during the ﬁrst few weeks of life. In a study by Sondhi et al.39 of 2271 newborns, 67% showed an exodeviation, 30% had essentially straight eyes, 2% swung between eso- and exodeviations, and only 1% had an esodeviation. By 2 months of age, all the esodeviations resolved, and 97% of exodeviations cleared by 6 months. Thus, almost all newborns have straight eyes or an exotropia, but esotropia is rare. The presence of an exodeviation at birth allows our innate strong fusional convergence to align the eyes. An esotropia, on the other hand, is more difﬁcult to control because fusional divergence is weak.

EYE MOVEMENT DEVELOPMENT AND SMOOTH PURSUIT ASYMMETRY Neonates typically have sporadic, jerky eye movements made up of saccadic eye movements without smooth pursuit. Initially, saccades are hypometric, but they continue to improve throughout infancy and childhood. Smooth pursuit eye movements develop after 4 to 6 weeks of age, with most infants having accurate smooth pursuit by 2 months of age. Horizontal smooth pursuit develops for targets moving in a temporal to nasal direction before pursuit movements in a nasal to temporal direction develop. This developmental lag in nasally directed smooth pursuit is called smooth pursuit asymmetry and is only seen under monocular conditions with one eye covered. During development, nasal to temporal pursuit movements are hypometric, requiring saccadic intrusion eye movements to keep up

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with the moving target.1 Smooth pursuit asymmetry can be detected clinically by testing monocular optokinetic nystagmus (OKN). Neonates will show a diminished OKN response with the drum rotating nasal to temporal as compared to temporal to nasal. Normally, smooth pursuit asymmetry becomes symmetrical between 4 to 6 months of age.31,32 If binocular visual development is disrupted during the ﬁrst few months of life (e.g., congenital esotropia and a unilateral cataract), smooth pursuit asymmetry and OKN asymmetry will persist throughout life.12,41,42,54,55 Smooth pursuit asymmetry does not interfere with normal visual function or the ability to read, as it is not present under binocular viewing. It is, however, an important phenomenon that shows a physiological link between ocular motor development and the development of binocular vision.

VISUAL DEVELOPMENTAL MILESTONES Central ﬁxation and accurate smooth pursuit are important clinical milestones of normal visual development (Table 4-2). Most children will show central ﬁxation and accurate smooth pursuit eye movements by 2 to 3 months of age, but some infants may show delayed visual maturation. Poor ﬁxation at 6 months of age is usually pathological, and should prompt a full evaluation

TABLE 4-2. Important Visual Developmental Milestones. Age

Visual Milestones

0–2 months

Pupillary response Sporadic ﬁx and follow Jerky saccadic eye movements Alignment: exodeviations common, but esodeviations rare Central ﬁx and follow (mother’s face) Accurate binocular smooth pursuit Monocular smooth pursuit asymmetry: temporally directed, slow; nasally directed, accurate optokinetic nystagmus (OKN) present Alignment: orthotropia with few exodeviations and no esodeviations Esotropia considered abnormal Central ﬁxation, reaches for toys and food Accurate and smooth pursuit eye movements Alignment: orthotropia 20/40 and not more than 2 Snellen lines difference 20/30 and not more than 2 Snellen lines difference

2–6 months

6 months–2 years

3–5 years 5 years

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for oculomotor or afferent visual pathway disease, including electrophysiology and neuroimaging studies.

Abnormal Visual Development A unilateral or bilateral blurred retinal image or strabismus will disrupt early visual development and can cause permanent visual loss. Following is a discussion of cortical suppression and amblyopia.

CORTICAL SUPPRESSION Strabismus, or a monocular blurred retinal image, causes dissimilar retinal images to fall on corresponding retinal areas of each eye. If the dissimilarity between the retinal images is great and the images cannot be fused, the visually immature adapts by inhibiting cortical activity from the blurred or deviated eye. This cortical inhibition usually involves the central portion of the visual ﬁeld and is termed cortical suppression. Images that fall within the ﬁeld of cortical suppression are not perceived, forming an area called a suppression scotoma. Suppression only occurs during binocular conditions with the dominant eye actively viewing or “ﬁxating” and disappears when the dominant eye is occluded. Suppression has been shown to reduce the ﬁrst positive peak (P-1) of the pattern visual evoked potential (P.VEP) (Fig. 4-2).58 The P-1 reﬂects early visual processing at the level of striate cortex, so it is likely that suppression occurs at, or before, the primary visual cortex. In Figure 4-2B, both eyes are open and the dominant eye is ﬁxing whereas the nondominant eye is stimulated with the pattern. There is no P-1 response from the nondominant eye because the visual activity from the ﬁxing eye cortically suppresses visual activity from the nondominant eye. Note that (in Fig. 4-2C) if the dominant eye is occluded in a patient with esotropia, there is no suppression and a high-amplitude P-1 is recorded from the nondominant eye. Cortical suppression interferes with the development of binocular cortical cells, resulting in abnormal binocular vision and poor, or no, stereoscopic vision. If suppression alternates between eyes, visual acuity will develop equally, albeit separately without normal binocular function. Constant suppression of one eye, on the other hand, not only results in poor binocularity but also causes poor vision (i.e., amblyopia).

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Check stimulus

No stimulus TV Monitor P-VEP Response

AMP

Amblyopic eye F ET

F

Occipital electrode

A

No response Fixing eye

B

Suppression amblyopic eye P-1

No suppression amblyopic eye Good response C FIGURE 4-2A–C. (A) Diagram of effect of suppression on the pattern visual evoked potential (P.VEP). The patient being tested has an esotropia and ﬁxates with the dominant right eye. An alternating check stimulus is presented to the deviated left eye during binocular viewing (B) and again to the left eye, but with the dominant right eye occluded (C). (B) The patient is ﬁxating with the dominant right eye and is cortically suppressing the deviated left eye. A check stimulus is presented to the deviated left eye, but there is no P.VEP response recorded when the right eye is ﬁxing because visual information from the left eye is cortically suppressed. (C) The dominant right eye is occluded and the left eye is stimulated, resulting in a high-amplitude P.VEP response. There is no suppression because the patient is monocularly ﬁxing with the left eye. The check stimulus now results in a robust cortical response from the left eye.

AMBLYOPIA Amblyopia occurs in approximately 2% of the general population and is the most common cause of decreased vision in childhood. The term amblyopia is derived from the Greek language and means dull vision: amblys dull, ops eye. Generally

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speaking, amblyopia can refer to poor vision from any cause but, in this volume and in most ophthalmic literature, amblyopia refers to poor vision caused by abnormal visual development secondary to abnormal visual stimulation. Other terms for this type of amblyopia include functional amblyopia and amblyopia ex anopsia. Children are susceptible to amblyopia between birth and 7 years of age.25 The earlier the onset of abnormal stimulation, the greater is the visual deﬁcit. The critical period for visual development is somewhat controversial but probably ranges from 1 week to 3 months of age. For practical purposes, amblyopia is deﬁned as at least 2 Snellen lines difference in visual acuity between the eyes, but amblyopia is truly a spectrum of visual loss, ranging from missing a few letters on the 20/20 line to hand motion vision. Functional amblyopia, or “amblyopia,” should be distinguished from organic amblyopia, which is poor vision caused by structural abnormalities of the eye or brain that are independent of sensory input, such as optic atrophy, a macular scar, or anoxic occipital brain damage. Functional amblyopia is reversible when treated with appropriate visual stimulation during early childhood, whereas organic amblyopia does not improve by visual stimulation.

Pathophysiology and Classiﬁcation of Amblyopia Amblyopia is caused by abnormal visual stimulation during visual development, resulting in abnormalities in the visual centers of the brain. There are two basic forms of abnormal stimulation: pattern distortion (i.e., blurred retinal image) and cortical suppression (i.e., constant suppression of one eye). Pattern distortion and cortical suppression can occur independently or together to cause amblyopia in the visually immature. Amblyopia can be created by blurring one or both retinal images or by inducing strabismus in visually immature animals (Fig. 4-3). Strabismus will cause amblyopia in infant animals if the animal ﬁxates with one eye and constantly suppresses the fellow eye. Strabismic animals that alternate ﬁxation do not develop amblyopia; however, they do not develop binocular vision. Pathological changes associated with induced amblyopia in the animal model occur in the lateral geniculate nucleus (LGN) and the striate cortex.20,21,23,24,44,48,49 Figure 4-4 shows the pathological changes in the lateral geniculate nucleus of a monkey raised

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with a monocular blurred retinal image. Normally, there are six nuclear layers of the LGN: three layers corresponding to the right eye and three layers corresponding to the left eye. Because of the blurred retinal image, only three layers corresponding to the eye with the clear retinal image developed. Due to the increased visual stimulation of the good eye, these three layers are darker stained and larger than normal.57 Ocular dominance columns in the striate cortex are also damaged as a result of a unilateral blurred image during early development (Fig. 4-4B).21 Von Noorden46,47 bridged the gap between human and animal research when he identiﬁed similar neural anatomic changes in a pathological study of humans with anisometropic amblyopia and strabismic amblyopia. Thus, this evidence has shown that the poor vision found with amblyopia is caused by brain damage. Clinically, amblyopia is associated with strabismus and strong ocular dominance (monocular suppression), a unilateral blurred retinal image secondary to refractive error or media opacity (pattern distortion and suppression), and bilateral blurred retinal images (bilateral pattern distortion). Table 4-3 lists a classiﬁcation of amblyopia based on etiology.

Strabismic Amblyopia Amblyopia can occur in patients with a constant tropia who show strong ﬁxation preference for one eye and constantly suppress cortical activity from the deviated eye. Amblyopia can also occur despite the fact that both eyes have clearly focused retinal images. Patients with strabismus who alternate ﬁxation and alternate suppression do not have amblyopia, but they do have abnormal binocular function. The mechanism for strabismic amblyopia is constant cortical suppression that degrades neuronal connections to the deviated eye. Strabismic amblyopia occurs in approximately 50% of patients with congenital esotropia (a constant tropia), but is very uncommon in patients with intermittent strabismus (e.g., intermittent exotropia) or those with incomitant strabismus (e.g., Duane’s syndrome and Brown’s syndrome) as they maintain central fusion by adopting a compensatory face turn. Strabismic amblyopia can be moderate to severe, and in some cases even results in visual acuity of 20/200 or worse.

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FIGURE 4-3. Diagram of cortical sensory adaptation to various visual stimuli during early visual development in the cat. Bars indicate percentage of occipital cortical cells that are either monocular cells, connected to the right eye (R) or left eye (L), or binocular cells, connected to both eyes (B). First column, normal visual development, no amblyopia or strabismus. Note that the majority of cortical cells are binocular, and the right and left eye monocular cell populations are equal. Second column, cortical adaptation to alternating esotropia. Note that the monocular cortical cells of left and right eye are now in the majority and there are relatively few binocular cells. There is no amblyopia, however, as the right and left eye monocular cell populations are equal. Third column, effect of a left esotropia with strong preference for the right eye so the left eye is amblyopic. The majority of cortical cells are right eye monocular cells, and there is a severe reduction of monocular left eye cells and binocular cells. Fourth column, effect of monocular pattern distortion by blurring the vision of the left eye with atropine. Left eye is amblyopic so it has the lowest representation, and the majority of cortical cells are connected to the right eye. Note that the binocular cells are diminished from normal but are relatively well preserved because of peripheral fusion; this is analogous to the monoﬁxation syndrome associated with anisometropic amblyopia. Fifth column, effect of equal pattern distortion to both eyes by blurring vision in both eyes with atropine. Both eyes become amblyopic, but the binocular cortical representation is essentially normal with the majority of cortical cells being binocular, and the left and right eye control similar numbers of monocular cells; this is analogous to ametropic amblyopia. (From Ref. 24, with permission.)

111

A

B1 FIGURE 4-4A,B. (A) Pathology of amblyopia (LGN): Cross-section of lateral geniculate nucleus (LGN) from a normal monkey (left ﬁgure) vs. amblyopic monkey caused by a unilateral blurred image (right ﬁgure). Note that the normal LGN has 6 nuclear layers (darkly stained cell layerleft ﬁgure) and the amblyopic LGN has only 3 layers, and they are thicker than normal (right ﬁgure).56,57

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B2 FIGURE 4-4A,B. (B) Pathology of amblyopia in monkey striate cortex (visual cortex). Well-deﬁned cortex dominance columns are seen in normal specimen (B1 ﬁgures), but cortex columns are underdeveloped in specimen for amblyopic monkey (B2 ﬁgures).21

Unilateral Pattern Distortion Amblyopia Unilateral, or asymmetrical, retinal image blur can produce amblyopia and loss of binocularity depending on the severity of the condition. The ophthalmic literature often refers to amblyopia associated with monocular image blur as “pattern deprivation amblyopia.” This term is misleading, because unilateral image blur results in pattern distortion and cortical suppression, both of which contribute to the amblyopia. Clinically, mild image blur (e.g., blur associated with mild anisometropia) causes mild anisometropic amblyopia and allows for the development of peripheral fusion and stereopsis (i.e.,

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TABLE 4-3. Classiﬁcation of Amblyopia. A. Strabismic amblyopia (suppression) 1. Congenital esotropia 2. Congenital exotropia 3. Acquired constant tropia in childhood 4. Accommodative esotropia 5. Small-angle tropia (monoﬁxation syndrome) 6. Intermittent exotropia (rarely associated with amblyopia) B. Monocular pattern distortion (suppression and pattern distortion) 1. Anisometropia a. Hyperopia 1.50 b. Myopia 3.00 c. Meridional 1.50 2. Media opacities a. Unilateral cataract b. Unilateral corneal opacity (Peter’s anomaly) c. Unilateral vitreous hemorrhage or vitreous opacity C. Bilateral pattern distortion (pattern distortion) 1. Ametropia a. Bilateral high hypermetropia 5.00 b. Bilateral meridional (astigmatic) 2.50 2. Media opacity a. Bilateral congenital cataracts b. Bilateral corneal opacities (Peter’s anomaly) c. Bilateral vitreous hemorrhages

monoﬁxation syndrome). A signiﬁcant blurred image during infancy (e.g., unilateral congenital cataract or corneal opacity), however, can result in severe amblyopia. Vision can be as poor as count ﬁngers with total loss of binocular function manifested by the development of sensory strabismus. Anisometropic amblyopia, one of the most common types of amblyopia, is caused by a difference in refractive errors that results in a unilateral or asymmetrical image blur. Most patients with anisometropic amblyopia have straight eyes and appear “normal,” so the only way to identify these patients is through vision screening. Stereoacuity testing has had limited value in screening for anisometropic amblyopia because most patients have relatively good stereopsis (between 70 and 3000 s arc). Patients with anisometropic amblyopia usually have peripheral fusion, and most have the monoﬁxation syndrome.35 Myopic anisometropia is generally less amblyogenic than hypermetropic anisometropia. As little as 1.00 hypermetropic anisometropia and 2.00 myopic anisometropia can be associated with amblyopia.51 Astigmatic anisometropic amblyopia does not occur unless there is a unilateral astigmatism greater than 1.50 D.51

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For practical purposes, however, we do not see signiﬁcant anisometropic amblyopia unless differences between the two eyes are greater than 1.50 in hyperopes and greater than 3.00 in myopes. Myopic anisometropic amblyopia is often amenable to treatment even in late childhood whereas hypermetropic amblyopia is often difﬁcult to treat past 4 or 5 years of age, probably because high myopia is usually acquired after the critical period of visual development, and the more myopic eye is in focus for near objects (a baby’s world is up close). In contrast, patients with hypermetropic anisometropia always use the less hypermetropic eye because it requires less accommodative effort and constantly suppress the more hypermetropic eye.

Bilateral Blurred Retinal Image Pattern distortion in its pure form without suppression occurs when there is bilateral symmetrical image blur and no strabismus. Clinically, the effects of pure image blur are seen in cases of bilateral high hypermetropia or bilateral symmetrical astigmatism, or with bilateral ocular opacities such as bilateral congenital cataracts and bilateral Peter’s anomaly. Bilateral pattern distortion causes bilateral poor vision. Depending on the extent of the distortion, some binocular fusion can develop, usually associated with gross stereopsis. If severe image blur occurs during the neonatal period so that essentially no pattern stimulation is provided, extremely poor vision and sensory nystagmus develop. Bilateral amblyopia and nystagmus will occur in cases of dense bilateral congenital opacities unless the image is cleared by 2 months of age. This type of nystagmus is called sensory nystagmus and is associated with bilateral severe amblyopia, or other causes of congenital blindness such as macular or optic nerve pathology. Sensory nystagmus does not occur with cortical blindness because extrastriate visual pathways anterior to the occipital cortex supply the ﬁxation reﬂex. Acquired opacities after 6 months of age usually do not cause sensory nystagmus because the motor component of ﬁxation has already been established. The presence of sensory nystagmus indicates severe amblyopia, usually 20/200 visual acuity or worse. Ametropic amblyopia (bilateral hypermetropic amblyopia) usually occurs with hypermetropia greater than 5.00 D without signiﬁcant anisometropia.36 In these cases, visual acuity is decreased in each eye, the eyes are usually straight, and the patients usually have gross stereopsis. When patients are ﬁrst

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given their optical correction, visual acuity does not signiﬁcantly improve. The lack of improvement with spectacle correction often leads the examiner to seek an organic cause for the decreased vision. The treatment of bilateral high hypermetropic amblyopia is to prescribe full hypermetropic correction. In most cases, visual acuity will slowly improve if the glasses are worn full-time, with ﬁnal visual acuity usually in the range of 20/30 to 20/25 achieved over a period of 6 months to a year. Bilateral meridional amblyopia is caused by bilateral astigmatism and, like bilateral hypermetropic amblyopia, is secondary to pattern distortion. Signiﬁcant meridional amblyopia occurs with astigmatism greater than 2.50 D. To avoid meridional amblyopia, astigmatisms of 2.50 D or more should be treated in preschool children, and astigmatisms over 3.00 D to 4.00 D should be treated in infants.

Amblyopic Vision The visual deﬁcit associated with amblyopia has certain unique characteristics, including the crowding phenomenon, the neutral density ﬁlter effect, and eccentric ﬁxation. The crowding phenomenon relates to the fact that patients with amblyopia have better visual acuity reading single optotype than reading multiple optotypes in a row (linear optotypes). Often, patients with amblyopia will perform 1 or 2 Snellen lines better when presented with single optotypes versus linear optotypes. This crowding phenomenon may have something to do with the relatively large receptive ﬁeld associated with amblyopia. Crowding bars are often used around a single optotype to provide a more sensitive test for amblyopia. A neutral density ﬁlter reduces overall luminance without inducing a color change. Decreased luminance of the visual target results in diminished central acuity in normal eyes. Decreased illumination of visual targets has less of an effect on amblyopic eyes because they are not using central acuity. The intraocular differences in visual acuity between the amblyopic eye and the sound eye diminish when the patient looks through a neutral density ﬁlter that lowers the luminance of the visual target. For example, a patient with a left amblyopia has 20/20 vision in the right eye and 20/60 in the left eye under photopic conditions (4 lines difference). He may have visual acuities of 20/50 right eye and 20/60 left eye under scotopic conditions (1 line difference).

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A

B FIGURE 4-5A,B. Eccentric ﬁxation. (A) Sound eye ﬁxes with the fovea (left) and the amblyopic eye eccentrically ﬁxates in an area of ﬁxation (right). (B) Right eye is covered, and eccentric ﬁxation persists with patient viewing in an eccentric area.

All amblyopes have some degree of extrafoveal ﬁxation. Mild amblyopes (20/40–20/100) ﬁxate so close to the fovea that they appear to ﬁxate centrally. Severe amblyopes, usually 20/200 to count ﬁngers, use a large parafoveal area for viewing (Fig. 45). This area of eccentric ﬁxation is not a pinpoint location but a general area of viewing. The presence of eccentric ﬁxation is a clinical sign of severe amblyopia and has a poor visual prognosis. Remember that anomalous retinal correspondence is quite different from eccentric ﬁxation. Anomalous retinal correspondence (ARC) is a binocular sensory adaptation to strabismus that allows acceptance of images on noncorresponding retinal points. ARC is only active during binocular viewing and, when one eye is covered, ﬁxation reverts back to the true fovea. Eccentric ﬁxation, on the other hand, is dense amblyopia without foveal ﬁxation and is present under monocular or binocular conditions.

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DIAGNOSING AMBLYOPIA Visual Acuity Testing When evaluating for amblyopia, linear acuity is more desirable than single optotype presentation because single optotype presentation underestimates the degree of amblyopia. Surround bars have been used to create crowding in a single optotype and are useful in children who get confused with the multiple optotypes used in linear acuity testing. There are many ways to test visual acuity in preschool children, including Allen picture ﬁgures, LEA ﬁgures, HOTV, illiterate E game, and the recently developed Wright ﬁgures©. The Wright ﬁgures are composed of black and white bars with a constant gap throughout the ﬁgure (Fig. 4-6). A recent study using the Wright ﬁgures on the Portal Stimuli System (Haag-Streit) found that the Wright ﬁgures tested two-point discrimination acuity, similar to Snellen acuity. Another advantage of the Wright ﬁgures is that their overall shape or footprint is similar for all ﬁgures, which prevents the child from determining the ﬁgure by the shape rather than internal two-point discrimination. (Dr. Wright collaborated with Gregg and Paul Podnar from Accommodata, Inc., Cleveland, OH, developers of the Portal System, to reﬁne the ﬁgures for use in this system and perform the study.) Visual acuity can often be measured in children as young as 2 to 3 years of age using preschool optotypes.

FIGURE 4-6. Wright ﬁgures consist of black and white bars with constant thickness and white gaps. The overall shape or footprint is similar for all ﬁgures, which prevents the child from determining the ﬁgure by the shape alone. The Wright ﬁgures correlate well with Snellen acuity. © 2000 by Dr. Kenneth W. Wright.

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Fixation Testing for Amblyopia Preverbal children can be tested for amblyopia by examining the quality of monocular ﬁxation or binocular ﬁxation preference.

MONOCULAR FIXATION TESTING Normally developed children more than 2 to 3 months of age should show central ﬁxation with accurate smooth pursuit and saccadic reﬁxation eye movements. Test for central ﬁxation by covering one of the patient’s eyes, then move a target slowly back and forth in front of the child to observe the accuracy of ﬁxation. A child with central ﬁxation looks directly at the target, visually locks on the target, and accurately follows the moving target. Infants often ﬁnd the human face a much more compelling target than toys or pictures, so try moving your head side to side to evaluate the quality of ﬁxation. Central ﬁxation indicates foveal vision usually in the range of 20/100 or better.

ECCENTRIC FIXATION Eccentric ﬁxation means the fovea is not ﬁxating and the patient is viewing from an extrafoveal part of the retina (Fig. 4-5). Patients with eccentric ﬁxation appear to be looking to the side, not directly at the ﬁxation target. They have poor smooth pursuits, so they do not accurately follow a moving target.

VISUSCOPE One way to identify the eccentric ﬁxation point in older cooperative children is to use a Visuscope, which is a type of direct ophthalmoscope that projects a focused image onto the retina so the examiner can see the image on the retina. First, the image is projected onto the parafoveal retina, then the patient is asked to look at the image. If the patient has central ﬁxation, the patient reﬁxates to place the image precisely on the fovea. However, with eccentric ﬁxation, the patient will view with the parafoveal retinal area and show a wandering, unsteady ﬁxation (see Fig. 4-5). The more peripheral the eccentric ﬁxation, the denser the amblyopia.

FIXATION PREFERENCE TESTING Testing for ﬁxation preference is useful in preverbal strabismic children to identify amblyopia that might be missed by mono-

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cular ﬁxation testing. It is based on the premise that strong ﬁxation preference indicates amblyopia. If a patient with strabismus spontaneously alternates ﬁxation, using one eye, then the other, this indicates equal ﬁxation preference and no amblyopia (Fig. 4-7).

A

B FIGURE 4-7A,B. Infant with congenital esotropia and alternating ﬁxation. Alternating ﬁxation indicates equal visual preference; no amblyopia. (A) Patient is ﬁxing with the left eye. (B) Patient has switched ﬁxation to the right eye.

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FIGURE 4-8. Measuring ﬁxation preference. Patient has strong ﬁxation preference for the left (left ﬁgure) and amblyopia in the right eye. Temporarily covering the left eye (center ﬁgure) forces ﬁxation to the right eye, but when the cover is removed, the patient reﬁxates to the left eye (right ﬁgure). This indicates strong ﬁxation preference, i.e., amblyopia.

Patients with a ﬁxation preference may have amblyopia. The strength of ﬁxation preference indicates if amblyopia is present, with the weaker preference for one eye being the amblyopic eye. Fixation preference can be quantiﬁed by brieﬂy covering the preferred eye to force ﬁxation to the nonpreferred eye. Remove the cover from the preferred eye, then observe how well and how long the patient will maintain ﬁxation with the nonpreferred eye before reﬁxating back to the preferred eye. If ﬁxation immediately goes back to the preferred eye after the cover is removed, then this indicates strong ﬁxation preference for the preferred eye and amblyopia of the deviated eye (Fig. 4-8). However, if the patient maintains ﬁxation with the nonpreferred eye through smooth pursuit, through a blink, or for at least 5 s, there is mild ﬁxation preference and no signiﬁcant amblyopia (vision within 2 Snellen lines difference) (Fig. 4-9). The ability to maintain ﬁxation with the nonpreferred eye while following a moving target is a very reliable indicator of equal vision and detects no signiﬁcant amblyopia. The reliability of ﬁxation preference testing for diagnosing amblyopia has been shown to be quite good in patients with large-angle strabismus, more than 10 to 15 PD.62 Patients with small-angle strabismus, however, will show strong ﬁxation

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FIGURE 4-9. Patient prefers to ﬁx with the left eye (left ﬁgure). Occluding left eye forces ﬁxation to right eye (center ﬁgure), and when the occluder is removed (right ﬁgure), the patient maintains ﬁxation with the nonpreferred eye, indicating no amblyopia.

preference in 50% to 70% of cases, even if the vision is equal to within a 2 Snellen lines difference.63,64 This high overdiagnosis rate in children with small-angle strabismus occurs because they have monoﬁxation syndrome. These patients have peripheral fusion but suppress one fovea, so they show strong ﬁxation preference even if vision is equal. The overdiagnosis of amblyopia in patients with small-angle strabismus can be rectiﬁed by using the vertical prism test, which disrupts peripheral fusion and temporarily breaks down the monoﬁxation syndrome.

VERTICAL PRISM TEST (INDUCED TROPIA TEST, 10 DIOPTER FIXATION TEST) The vertical prism test is used in preverbal children with straight eyes or small-angle strabismus to accurately diagnose amblyopia.62,63 It is performed by placing a 10 to 15 PD prism base-up or base-down in front of one eye, thereby inducing a vertical tropia (Fig. 4-10). With the induced vertical strabismus, ﬁxation preference can be determined as shown in Figure 4-11. In Figure 4-11A, a base-down prism is placed over the right eye. The right eye is ﬁxing because both eyes move up as the right eye ﬁxates through the prism. In Figure 4-11B, the prism is placed over the left eye, but the patient still ﬁxates with the right eye, evidenced by the fact that both eyes are in primary

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position, ignoring the prism in front of the left eye. If the patient can hold ﬁxation with either eye through a blink or through smooth pursuit eye movements, no signiﬁcant amblyopia is present. A strong ﬁxation preference indicates amblyopia.

CROSS-FIXATION Patients with a large-angle esotropia and tight medial rectus muscles will have difﬁculty bringing the eyes to primary position, so the eyes stay adducted. These patients “cross-ﬁxate.” The right adducted eye ﬁxes on objects in left gaze, and the left adducted eye ﬁxates on objects in right gaze. Cross-ﬁxation has been said to be a sign of equal vision, but cross-ﬁxation does not guarantee that a patient sees equally with each eye. The ability to hold ﬁxation past midline or to hold ﬁxation through smooth pursuit with either eye is a better criterion for equal vision.

LATENT NYSTAGMUS Patients with strabismus often have latent nystagmus, which is a horizontal jerk nystagmus that occurs or gets worse in both eyes if one eye is occluded. Thus, covering one eye in a patient with latent nystagmus will increase nystagmus and diminish visual acuity. To evaluate monocular visual function, blur one

FIGURE 4-10. Vertical prism test of a patient ﬁxing with the left eye because of a right amblyopia. A vertical prism is placed in front of the left eye and, because the left eye is ﬁxing, the left eye elevates to pick up the ﬁxation. As per Hering’s law, both eyes will elevate if the left eye is ﬁxing.

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A

B FIGURE 4-11A,B. (A) Vertical prism is placed in front of one eye to identify which eye is ﬁxing, and therefore ﬁxation preference can be determined. (A) One can identify that the right eye is ﬁxing because the right eye is in primary position and the patient is ignoring the vertical displaced image in the left eye. (B) Patient is still ﬁxing with the right eye. Both eyes shift upward because the right eye is viewing through the prism. This is a base-down prism, so the eyes move up.

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eye with a plus lens rather than occluding one eye. Blurring one eye induces less nystagmus than occlusion. Use the minimum amount of plus necessary to force ﬁxation to the fellow eye. The vertical prism test can identify which eye is ﬁxing. Usually, a 5.00 D lens is sufﬁcient to blur distance vision enough to force ﬁxation to the fellow eye. Linear presentation of optotypes is difﬁcult for patients with nystagmus because the optotypes tend to run together, so try a single optotype presentation. Also, take a binocular visual acuity measurement in addition to a monocular acuity in patients with nystagmus because binocular vision is usually better than monocular vision. To assess the best functional visual acuity potential in a patient with nystagmus, test binocular vision while allowing the patient to adopt their preferred face turn or head tilt.

VISION SCREENING Early detection and treatment of pediatric ocular disease is critical. Diseases such as congenital cataracts, retinoblastoma, and congenital glaucoma require early treatment during infancy. Delay in diagnosis may result in irreversible vision loss and, in the case of retinoblastoma, even death. Patients with congenital cataracts treated during the ﬁrst weeks of life have a relatively good prognosis, whereas surgery performed after 2 to 3 months of age is considered late and is associated with a poor visual outcome. It is, therefore, imperative to perform effective vision screening for all children from newborn infants to older children. Vision screening examinations should start at birth and continue as part of routine checkups for primary care physicians. The acronym I-ARM (inspection—acuity, red reﬂex, and motility) can be a helpful reminder of the essential parts of a pediatric screening examination. Table 4-4 summarizes the I-ARM screening eye examination for neonates, babies, and children. The most important test for the newborn is the red reﬂex test. If an abnormal red reﬂex is present, then an immediate referral to an ophthalmologist is required. Infant screening examinations take less than a minute, but this brief exam is quite powerful. If performed properly, it can detect the vast majority of eye pathology, including the important diagnoses mentioned previously. Guidelines for visual acuity referral are presented in Table 4-5.

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TABLE 4-4. Screening Eye Examination: I–ARM. Neonate (Birth–2 months)

Babies (3 months–2 years)

Children (3 years and older)

Symmetry Face & eyes Poor ﬁxation Pupillary response

Face turn or head tilt

Face turn or head tilt

Good ﬁxation and smooth pursuit

Red reﬂex

Red reﬂex test

Motility

Gross alignment (70% small exotropia but esotropia probably abnormal

Binocular red reﬂex (Brückner) Good alignment Light reﬂex and Brückner (esotropia is abnormal after 2 months of age)

Visual acuity: Allen cards, E-game, Snellen acuity Bilateral red reﬂex test (Brückner) Good alignment Light reﬂex and Brückner (any misalignment is abnormal)

Steps Inspection Acuity

Red Reﬂex The red reﬂex test is the single best vision screening exam for infants and young children. It is best performed using the Brückner modiﬁcation, which is simply a simultaneous bilateral red reﬂex. Use the direct ophthalmoscope and view the patient’s eyes at a distance of approximately 2 feet from the patient. Use a broad beam so that both eyes are illuminated at the same time. Dim the room lights and have the child look directly into the ophthalmoscope light. Start with the ophthalmoscope on low illumination then slowly increase the illumination until a red reﬂex is seen. You will observe a red reﬂex that ﬁlls the pupil and a small (approximately 1 mm) white light reﬂex that appears to reﬂect off the cornea (Fig. 4-12). The white light reﬂex is actually a reﬂex coming from just behind the pupil and is called the “corneal light reﬂex” or the “Hirschberg reﬂex.” Thus, the Brückner test gives both a red reﬂex and the corneal light reﬂex simultaneously. Blockage of the retinal image or large retinal pathology will result in an abnormal red reﬂex. A cataract can either block the

TABLE 4-5. Abnormal Red Reﬂex: Symmetry Is the Key. Cataract Vitreous hemorrhage Retinoblastoma Anisometropia Strabismus

May block the red reﬂex (dark or dull reﬂex) or may look white (leukocoria) Blocks red reﬂex (dark or dull reﬂex) Appears as a yellow or white reﬂex (leukocoria) Results in an unequal red reﬂex Causes a brighter red reﬂex in the deviated eye; the corneal light reﬂex will be decentered

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FIGURE 4-12. Normal Brückner test with symmetrical red reﬂex and centered corneal light reﬂex.

red reﬂex or reﬂect light to give a white reﬂex. Retinoblastoma has a yellowish-white color and will produce a yellow reﬂex. Anisometropia (difference in refractive error) will result in an unequal red reﬂex. Strabismus will cause a brighter red reﬂex in the deviated eye, and the corneal light reﬂex will be decentered. The key sign of a normal exam is symmetry. See Figure 4-13 and Table 4-5 for examples of abnormal red reﬂexes.

AMBLYOPIA TREATMENT Early treatment of amblyopia is critical for best visual acuity results. The basic strategy for treating amblyopia is to ﬁrst provide a clear retinal image, and then correct ocular dominance if dominance is present, as early as possible during the period of visual plasticity (birth to 8 years). Correction of ocular dominance is accomplished by forcing ﬁxation to the amblyopic eye through patching or blurring the vision of the sound eye.

Clear Retinal Image Patients with bilateral hypermetropia (5.00 D) should receive the full hypermetropic correction, as amblyopic eyes do not fully accommodate. Patients who are given partial correction of their high hypermetropia often show very slow or no improvement

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A

B FIGURE 4-13A,B. Abnormal reﬂex. (A) Cataract: left eye. sometropia: brighter reﬂex in right eye.

(B) Ani-

in their amblyopia. Patients with large astigmatism (2.50 D) will also have amblyopia secondary to the astigmatism or develop meridional amblyopia. Prescribe the full astigmatic correction to provide a clear retinal image. It is important to consider correcting astigmatisms of 2.50 to 3.00 or more in small children, even if the astigmatism is bilateral. Table 4-6 lists guidelines for prescribing spectacles in children. In general, if the patient has anisometropic amblyopia and straight eyes, this author initially prescribes just glasses and waits to start patch-

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C FIGURE 4-13C. (C) Strabismus: esotropia with brighter reﬂex from deviated left eye. (Note: This is the author’s youngest son. The author subsequently performed strabismus surgery on him, and the eyes have remained straight.)

ing of the good eye. Most anisometropic amblyopes will respond to glasses alone with no or minimal part-time occlusion of the good eye.19 Children with media opacities, such as a visually signiﬁcant cataract, should have immediate surgery with visual rehabilitation using a contact lens or intraocular lens. Early treatment is critical; infants with a congenital cataract should undergo surgery within the ﬁrst month of life, even as early as the ﬁrst week. TABLE 4-6. When Should Spectacles Be Prescribed in Children? Type of refractive error Hypermetropic anisometropia Myopic anisometropia Astigmatic anisometropia Bilateral hypermetropia Bilateral astigmatism

Threshold for prescribing spectacles 1.50 3.00 1.50 5.00 2.50

D D D D D

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Correct Ocular Dominance OCCLUSION Patching or occlusion therapy is based on covering the sound eye to stimulate the amblyopic eye. Strabismic patients without binocular fusion can be treated with full-time occlusion; however, full-time occlusion may result in reverse amblyopia in children under 4 to 5 years of age. To prevent reverse amblyopia, do not use full-time occlusion for more than 1 week per the child’s age in years without reexamining the vision of the good eye. For example, a 2-year-old child receiving full-time occlusion should be examined every 2 weeks. In children less than 1 year of age, part-time occlusion may be preferable to avoid reverse amblyopia. Amblyopic patients with essentially straight eyes (tropias 8 PD) and peripheral fusion (e.g., anisometropic amblyopia and microtropia monoﬁxators) are best treated with part-time patching (3 to 4 h/day) or no occlusion. For anisometropic amblyopia, initially prescribe spectacle correction and follow the patient each month for visual acuity improvement. If vision does not improve on monthly follow-ups, then part-time patching is started. Part-time occlusion or penalization therapy is preferred because these methods help to preserve fusion. If vision does not improve with part-time occlusion, then full-time occlusion should be tried.

PENALIZATION Penalization is a method for blurring the sound eye to force ﬁxation to the amblyopic eye. Penalization actually switches ocular suppression, which can be demonstrated by a Polaroid vectographic chart or by the Worth 4-dot test. Penalization only works if ﬁxation is switched from the sound eye to the amblyopic eye.59 Blurring of the sound eye can be achieved by various methods. Optical penalization is based on over-plussing (prescribing more plus sphere than needed) the sound eye to force ﬁxation to the amblyopic eye for distance targets; the patient will usually use the sound eye for near targets. Optical penalization works well for mild amblyopia; however, some children will look over the tops of their glasses to use their sound eye. Atropine penalization is a stronger form of penalization and is useful even in dense amblyopia so long as the patient has signiﬁcant hypermetropia of the good eye.38 Atropine at 0.5% or

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1% is placed in the sound eye each day, optical correction is removed from the sound eye, and the amblyopic eye is given full optical correction. If the patient switches ﬁxation to the amblyopic eye under these conditions of penalization, then penalization will improve vision.59 Cyclopentolate can be used as an in-ofﬁce test to predict if penalization will work.59 The in-ofﬁce test consists of providing the amblyopic eye with full optical correction while deadening the sound eye with cyclopentolate and removing optical correction from the sound eye. If ﬁxation switches to the amblyopic eye under these conditions, then the patient will improve with atropine penalization. Atropine penalization usually requires 3.00 or more hypermetropia in the sound eye to obtain significant blur to switch ﬁxation. It is important to note that blurring the sound eye to a visual acuity lower than the amblyopic eye does not guarantee a switch in ﬁxation to the amblyopic eye. Penalization in young children may result in reverse amblyopia (decrease vision in the previously good eye), so patients 4 years of age or younger should be followed closely when undergoing atropine penalization therapy.50,59

OCCLUSIVE CONTACT LENS Occlusive contact lens can be used in treating amblyopia. A study by Eustis and Chamberlain15 showed 92% of patients improved at least 1 line of Snellen acuity, but complications limited the usefulness. Complications included conjunctival irritation and poor contact lens ﬁt, and one patient even learned to decenter the lens to peek around the occlusive contact lens. There was a high recurrence to pretreatment visual acuity, as 55% showed recurrence of amblyopia. The authors concluded that occlusive contact lenses should only be considered as a last resort and that these patients require close follow-up.15

BILATERAL LIGHT OCCLUSION A preventive treatment of amblyopia may be the use of bilateral light occlusion. Studies on dark-rearing have shown that bilateral total light occlusion prolongs the sensitive period of visual development. In several animal studies, researchers have shown that animals placed in total darkness for several months (or the human equivalent to several years) do not develop dense amblyopia and their visual development is minimally affected.9,10,11,40 A study by Hoyt22 on neonates with hyperbilirubinemia treated

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under bili-lights who were patched bilaterally from several days to 2 weeks showed that they did not have an increased incidence of amblyopia or strabismus. In a separate report by the author,61 a neonate received 17 days of bilateral patching after having 2 weeks of dense vitreous hemorrhage and hyphema. Follow-up at 3 years of age showed visual acuity of 20/30 in each eye and a small accommodative esophoria with good fusion. Bilateral light occlusion remains controversial and, in this author’s opinion, should be used only as a temporary measure in neonates 3 months or younger with ocular opacities such as congenital cataracts. Urgent surgery is still required but, for visually signiﬁcant cataracts, bilateral occlusion can be used to prevent amblyopia until the retinal image is cleared. The author’s recommendation is to limit bilateral patching to a maximum of 2 weeks.

LEVODOPA/CARBIDOPA IN THE OF AMBLYOPIA

TREATMENT

Levodopa/carbidopa has been traditionally used to treat Parkinson’s disease. Levodopa is a precursor for the catecholamine dopamine, a neurotransmitter/neuromodulator known to inﬂuence receptive ﬁelds. Levodopa/carbidopa has been studied as an adjunct to patching for the treatment of amblyopia.27,28,29,30 The treatment remains controversial, as the visual acuity improvement has been relatively small, not clearly better than with patching alone, and there are questions regarding long-term stability of vision.

PLEOPTICS Pleoptics is a method of treating eccentric ﬁxation associated with dense amblyopia. A bright ring of light is ﬂashed around the fovea to temporarily “blind” or saturate the photoreceptors surrounding the fovea, which eliminates vision from the eccentric ﬁxation point and forces ﬁxation to the fovea. Pleoptic treatments are given several times a week to enhance occlusion therapy. Most practitioners have found pleoptics to be no better than standard occlusion therapy.16

ACTIVE STIMULATION Some investigators have suggested active stimulation of the amblyopic eye as a way to improve vision in the amblyopic eye.

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A high-contrast spinning disc with square-wave grading was one method that has been tried (CAM). The CAM treatment has been found to be no better than standard occlusion therapy.8

PROGNOSIS OF AMBLYOPIA The prognosis for amblyopia depends upon the age of the patient, severity of amblyopia, and type of amblyopia. The earlier the amblyopia occurs and the longer it remains untreated, the worse the prognosis. In general, bilateral amblyopia responds better than unilateral amblyopia, and myopic anisometropic amblyopia responds better than hypermetropic anisometropic amblyopia. Each case must be evaluated individually as to whether the child is too old to undergo amblyopia therapy. Visual acuity improvement has been documented when children are treated in late childhood after 8 years of age.6,33 This author reported improvement in vision from legally blind to 20/70 and damping of sensory nystagmus in a 14-year-old who underwent late cataract surgery for bilateral congenital cataracts.60 Even adults with dense amblyopia can show visual acuity improvement and prolonged plasticity. Signiﬁcant visual acuity improvement of the amblyopic eye has been reported in adults who have lost vision in their good eye and relied on the amblyopic eye for their vision.14,45

References 1. Atkinson J. Development of optokinetic nystagmus in the human infant and monkey infant: an analogue to development in kittens. In: Freeman RD (ed) Developmental neurobiology of vision. New York: Plenum Press, 1979. 2. Birch EE, Gwiazda J, Held R. Stereoacuity development of crossed and uncrossed disparities in human infants. Vision Res 1982;22:507. 3. Birch E, Petrig B. FPL and VEP measures of fusion, stereopsis and stereoacuity in normal infants. Vision Res 1996;36(9):1321–1327. 4. Braddick O, et al. Cortical binocularity in infants. Nature (Lond) 1980;288:363–365. 5. Braddick O, Wattam-Bell J. The onset of binocular function in human infants. Hum Neurobiol 1983;2(2):65–69. 6. Brown MH, Edelman PM. Conventional occlusion in the older amblyope. Am Orthopt J 1976;26:54–56. 7. Carney T. Evidence for an early motion system which integrates information from the two eyes. Vision Res 1997;37(17):2361–2368.

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8. Crandall MA, Gerhard WC, Ellerhorst B. CAM (stripe) therapy for amblyopia, Perspect Ophthalmol 1981;5(1):51–55. 9. Cynader M, Berman N, Hein A. Recovery of function in cat visual cortex following prolonged deprivation. Exp Brain Res 1976:25:139– 156. 10. Cynader M, Mitchell DE. Prolonged sensitivity to monocular deprivation in dark-reared cats. J Neurophysiol 1980;43:1026– 1040. 11. Cynader M. Prolonged sensitivity to monocular deprivation in darkreared cats: effects of age and visual exposure. Dev Brain Res 1983; 8:155–164. 12. Demer JL, von Noorden GK. Optokinetic asymmetry in esotropia. J Pediatr Ophthalmol Strabismus 1988;25:286. 13. Daw N. Critical periods and amblyopia. Arch Ophthalmol 1998; 116(4):502–505. 14. Ellis FD, Schlaegel TF. Unexpected visual recovery: organic amblyopia? Am Orthopt J 1991;31:7. 15. Eustis HS, Chamberlain D. Treatment for amblyopia: results using occlusive contact lens. J Pediatr Ophthalmol Strabismus 1996;33: 319–322. 16. Fletcher MC, Silverman SJ, Boyd J, Callaway M. Biostatistical studies: comparison of the management of amblyopia by conventional patching, intensive hospital pleoptics, and intermittent ofﬁce pleoptics. Am Orthopt J 1969;19:40. 17. Fox R, Aslin RN, Shea SL, Dumais ST. Stereopsis in human infants. Science 1980;207:323. 18. Garey LJ, De Courten C. Structural development of the lateral geniculate nucleus and visual cortex in monkey and man. Behav Brain Res 1983;10:3–13. 19. Hakim OH, Wright KW. Treatment of anisometropic amblyopia with minimal or no patching. Abstracts Program #2148. ARVO, May/Ft. Lauderdale, FL. 2001. 20. Hendrickson AE, Movshon JA, Eggers HM, Gizzi MS, Boothe RG, Kiorpes L. Effects of early unilateral blur on the macaque’s visual system. II. Anatomical observations. J Neurosci 1987;7:1327– 1339. 21. Horton JC, Hocking DR. Timing of the critical period for plasticity of ocular dominance columns in macaque striate cortex. J Neurosci 1997;17(10):3684–3709. 22. Hoyt CS. The long-term visual effects of short-term binocular occlusion of at-risk neonates. Arch Ophthalmol 1980;98:1970. 23. Hubel KH, Weisel TN. Receptive ﬁeld, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol 1962;160: 106–154. 24. Ikeda H, Tremain K. Amblyopia and cortical binocularity. Trans Ophthalmol Soc UK 1980;100:452. 25. Keech RV, Kutschke PJ. Upper age limit for the development of amblyopia. J Pediatr Ophthalmol Strabismus 1995;32:89–93.

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26. Leguire LE, Rogers GL, Bremer DL. Visual-evoked response binocular summation in normal and strabismic infants. Investig Ophthalmol Vis Sci 1991;32:126–133. 27. Leguire LE, Rogers GL, Bremer DL, Walson P, HadjiconstantinouNeff M. Levodopa and childhood amblyopia. J Pediatr Ophthalmol Strabismus 1992:29:290–298. 28. Leguire LE, Rogers GL, Bremer DL, Walson P, McGregor ML. Levodopa/carbidopa for childhood amblyopia. Investig Ophthalmol Vis Sci 1993;34:3090–3095. 29. Leguire LE, Rogers GL, Bremer DL, Walson P, McGregor ML. Longitudinal study of levodopa/carbidopa for childhood ambylopia. J Pediatr Ophthalmol Strabismus 1993;30:354–360. 30. Leguire LE, Rogers GL, Bremer DL, Walson P, McGregor ML. Levodopa/carbidopa treatment for the amblyopia in older children. J Pediatr Ophthalmol Strabismus 1995;32:143–151. 31. Lewis TL, Maurer D, Brent HP. Optokinetic nystagmus in normal and visually deprived children: implications for cortical development. Can J Psychol 1989;43:121–140. 32. Naegele JR, Held R. The postnatal development of monocular optokinetic nystagmus in infants. Vision Res 1982;22:341. 33. Oliver M, et al. Compliance and results of treatment for amblyopia in children more than 8 years old. Am J Ophthalmol 1986;102:340– 345. 34. Ottar WL, Scott WE, Holgado SI. Photoscreening for amblyogenic factors. J Pediatr Ophthalmol Strabismus 1995;32:289–295. 35. Parks MM. The monoﬁxational syndrome. Trans Am Ophthalmol Soc 1969;67:609–657. 36. Raab E. Refractive amblyopia. Int Ophthalmol Clin 1971;II:155. 37. Rakic P. Prenatal genesis of connections subserving ocular dominance in rhesus monkey. Nature (Lond) 1976;261:467. 38. Repka MX, Ray JM. The efﬁcacy of optical and pharmacological penalization. Ophthalmology 1993;100:769–775. 39. Sondhi N, Archer SM, Helveston EM. Development of normal ocular alignment. J Pediatr Ophthalmol Strabismus 1988;25:210–211. 40. Timney B, Mitchell DE, Gifﬁn F. The development of vision in cats after extended periods of dark-rearing. Exp Brain Res 1978;31: 547–560. 41. Tychsen L, Lisberger SG. Maldevelopment of visual motion procession in humans who had strabismus with onset in infancy. J Neurosci 1986;6:2495–2508. 42. Tychsen L. Binocular vision. In: Hart WM (ed) Adler’s physiology of the eye: clinical applications, 9th edn. St. Louis: Mosby, 1992:773– 853. 43. Tychsen L, Boothe RG. Latent ﬁxation nystagmus and nasotemporal asymmetries of motion visually evoked potentials in naturally strabismic primate. J Pediatr Ophthalmol Strabismus 1996;33:148–152. 44. van Essen DC, Maunsell JHR. Hierarchical organization and functional streams in the visual cortex. Trends Neurosci 1983:6:370–395.

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45. Vereecken EP, Brabant P. Prognosis for vision in amblyopia after the loss of the good eye. Arch Ophthalmol 1984;102:220. 46. von Noorden GK, Crawford ML. The lateral geniculate nucleus in human strabismic amblyopia. Investig Ophthalmol Vis Sci 1992; 33(9):2729–2732. 47. von Noorden GK, Crawford MLJ, Levacy RA. The lateral geniculate nucleus in human anisometropic amblyopia. Investig Ophthalmol Vis Sci 1983;24:788–790. 48. von Noorden GK, Crawford MLJ. The effects of total unilateral occlusion vs. lid suture on the visual system of infant monkeys. Investig Ophthalmol Vis Sci 1981;21:142–146. 49. von Noorden GK, Crawford MLJ. Form vision deprivation without light deprivation produces the visual deprivation syndrome in Macaca mulatta. Brain Res 1977;129:37–44. 50. von Noorden GK. Amblyopia caused by unilateral atropinization. Ophthalmology 1981;88:131–133. 51. Weakley DR. The association between anisometropia, amblyopia and binocularity in the absence of strabismus. Trans Am Ophthalmol Soc 1999;48:987–1021. 52. Weinacht S, Kind C, Monting JS, Gottlob I. Visual development in preterm and full term infants: a prospective masked study. Investig Ophthalmol Vis Sci 1999;40(2):346–353. 53. Werner DB, Scott WE. Amblyopia case reports: bilateral hypermetropic ametropic amblyopia. J Pediatr Ophthalmol Strabismus 1985; 22:203–205. 54. Westall CA, Woodhouse JM, Brown VA. OKN asymmetries and binocular function in amblyopia. Ophthalmol Physiol Opt 1989;9: 269–276. 55. Westall CA, Eizenman M, Kraft SP, Panton CM, Chatterjee S. Cortical binocularity and monocular optokinetic asymmetry in early onset esotropia. Investig Ophthalmol Vis Sci 1998;39(8):1352– 1360. 56. Wiesel TN, Hubel DH. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 1963;26:1003– 1017. 57. Wiesel TN, Hubel DH. Ordered arrangement of orientation columns in monkeys lacking visual experience. J Comp Neurol 1974;158: 307. 58. Wright KW, Fox BES, Erikson KJ. PVEP evidence of true suppression in adult onset strabismus. J Pediatric Ophthalmol Strabismus 1990; 27:196–201. 59. Wright KW, Guyton DL. A test for predicting the effectiveness of penalization on amblyopia. In: Henkind P (ed) Acta: XXIV international congress of ophthalmology. Philadelphia: Lippincott, 1983: 896–901. 60. Wright KW, Christensen LE, Noguchi BA. Results of late surgery for presumed congenital cataracts. Am J Ophthalmol 1992;114(4):409– 415.

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61. Wright KW, Wehrle MJ, Urrea PT. Bilateral total occlusion during the critical period of visual development. Letter to the editor. Arch Ophthalmol 1987;105:321. 62. Wright KW, et al. Reliability of ﬁxation preference testing in diagnosing amblyopia. Arch Ophthalmol 1986;104:549–553. 63. Wright KW, Walonker F, Edelman P. 10-diopter ﬁxation test for amblyopia. Arch Ophthalmol 1981;99:1242–1246. 64. Zipf RF. Binocular ﬁxation pattern. Arch Ophthalmol 1976;94:401– 405.

5 The Ocular Motor Examination Kenneth W. Wright

EVALUATION OF THE STRABISMIC PATIENT The goals of the strabismus examination are to (1) diagnose amblyopia; (2) establish a strabismus diagnosis (e.g., pseudoesotropia, congenital esotropia, cranial nerve palsy, or restrictive strabismus); (3) assess the binocular status (e.g., bifoveal fusion, monoﬁxation–peripheral fusion, anomalous retinal correspondence, no fusion–large suppression, diplopia, and fusion potential); and (4) measure and characterize the deviation. A well-focused, goal-oriented evaluation helps prevent a laborious exhaustive examination that results in patient fatigue, examiner fatigue, and the collection of spurious data. Even after a full evaluation, a patient’s strabismus may not clearly fall into a speciﬁc category, and the diagnosis may be nebulous. In these cases, the patient can still be appropriately managed if evaluated for amblyopia, sensory status, size of the deviation, and the possibility of an underlying neurological problem or systemic disease. As in all aspects of medicine, the combination of detailed history and careful physical examination provides the foundation for making the correct diagnosis and taking the appropriate action.

HISTORY The character and onset of the strabismus provides information about binocular fusion potential. The earlier the onset and longer the duration of the strabismus, the worse the prognosis for binocular vision. Older children with congenital strabismus 138

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who have never experienced fusion have a poor fusion prognosis, whereas an acquired strabismus of a few months duration usually indicates the patient has developed at least some binocular vision and has the potential to recover binocular fusion. A history of compensatory head posturing speaks for binocular fusion, as does a history of an intermittent strabismus. In the real world of clinical practice, however, these general rules do not hold 100% of the time as some patients will obtain binocular fusion after late surgery for a presumed congenital strabismus. The history of an acquired strabismus is important because it may indicate a neurological or systemic disease, especially when the strabismus is incomitant and associated with limited ductions. An unexplained acquired incomitant strabismus requires neurological evaluation. Examining baby photographs, the family album, or a patient’s driver’s license under magniﬁcation can facilitate documenting the onset and type of strabismus. Additionally, patients should be questioned about the presence of diplopia, as diplopia usually indicates acquired strabismus with onset usually after 4 to 6 years of age. History regarding birth weight, complications of birth, the health of the child, and developmental milestones are also an integral part of a complete evaluation. Finally, the family history is very important. Although the exact hereditary pattern of strabismus is unclear, most types of strabismus are familial.

PHYSICAL EXAMINATION Try to obtain as much information as possible by inspection without touching the child. Use toys to play with the child to observe eye alignment and eye movements. Save the more intrusive parts of the examination for last. The steps for the strabismic examination are listed in order in Table 5-1. Traditionally, binocular sensory testing is performed before tests that require occluding one eye, such as visual acuity testing and the cover/ uncover tests. Covering one eye dissociates the eyes and may disrupt fusion in a patient with latent strabismus (large phoria or intermittent tropia). This may be more of a theoretical consideration, as Biedner et al.2 found no signiﬁcant difference in stereopsis tested at the beginning versus at the end of the exam. This author prefers testing vision early, before sensory testing, as knowledge of the visual acuity sets the tone for the rest of the examination.

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TABLE 5-1. Order of Examination. 1. 2. 3. 4. 5. 6. 7. 8.

Inspection: Evaluation and measurement of face turns Amblyopia assessment/visual acuity Sensory tests (see Chapter 6) Ductions and versions Measurement of deviation Special tests for identifying restriction and paresis Cycloplegic refraction Fundus examination (objective torsion)

ORDER OF EXAMINATION Inspection The physical examination actually starts as the patient enters the room. While taking the history, it is important to observe the patient’s visual behavior, eye alignment, eye movements, ﬁxation, and head posturing. By the time the history is recorded, a good observer will often have established a preliminary differential diagnosis. An initial differential diagnosis helps guide the direction of the physical examination and minimize extraneous test. However, be careful not to overanticipate: keep an open mind. Much can be learned about the patient’s sensory status from simple inspection. Do the eyes appear straight? Is there a face turn or head posturing? The presence of straight eyes with a face turn in a patient with strabismus can indicate the presence of binocular fusion even if this cannot be demonstrated by sensory testing. Often, patients with weak fusion will break down to a tropia after even a brief cover test or during sensory tests. Therefore, it is important to observe the patient’s alignment and face posturing before formal testing.

Amblyopia Assessment/Visual Acuity Techniques for diagnosing amblyopia are covered in Chapter 4. Always try to document visual function even in neonates or developmentally delayed children who are unable to cooperate with standard testing. Preverbal children can be tested for amblyopia by examining the quality of monocular ﬁxation or binocular ﬁxation preference. When evaluating amblyopia in older cooperative children, use linear acuity because single opto-

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type presentation lacks crowding and slightly underestimates the degree of amblyopia. In young preliterate children, however, single optotype testing is quicker, easier, and probably more accurate than linear optotypes. Crowding bars around an optotype or using the Wright ﬁgures have inherent crowding and may be useful for diagnosing amblyopia with single optotypes. There are many ways to test visual acuity in preschool children including Wright ﬁgures, Allen picture cards, HOTV, and the illiterate E game.

Sensory Tests A description of sensory tests is provided in Chapter 6. Evaluation of the sensory status should be part of every strabismus examination and usually includes a haploscopic fusion/suppression test (e.g., Worth 4-dot test) and a test for stereoacuity (e.g., Titmus).

Ductions and Versions Ductions test monocular movements and are examined with one eye occluded, forcing ﬁxation to the eye being examined. Ductions evaluate the ability for the eye to move into extreme ﬁelds of gaze. Figure 5-1 shows both normal and limited abduction; this is a scale of 0 to 4, with 1 limitation meaning slight limitation and 4 indicating severe limitation with inability of the eye to move past midline. This scale can be used to measure horizontal and vertical ductions. Versions test binocular eye movements and show how well the eyes move together in synchrony. Versions will detect subtle imbalance of eye movements and oblique muscle dysfunction missed on ductions. Evaluation of versions should include eye movements through the nine cardinal positions of gaze: from primary position to straight right, straight left, straight up, straight down, up to the right, up to the left, down to the right, and down to the left (Fig. 5-2). Abnormal versions can be noted on a scale of 4 to 4 with 0 indicating normal and 4 indicating maximum overaction (Fig. 5-3A), whereas 4 indicates severe underaction (Fig. 5-3B). It is important to remember, when observing for oblique dysfunction, to make sure the abducting eye is ﬁxing so the adducting eye is free to manifest the oblique dysfunction; this can be accomplished by partially occluding the adducting eye (with your thumb or occluder) and

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A

B

C

D E FIGURE 5-1A–E. Ductions are monocular eye movements: (A) normal abduction; (B) 1 limitation to abduction; (C) 2 limitation to abduction; (D) 3 limitation to abduction; (E) 4 limitation to abduction. This scheme is used to quantitate limitation of duction movements and can be used for abduction or vertical ductions as well.

FIGURE 5-2. Versions are binocular eye movements: dextroversion, rightgaze; levoversion, leftgaze; superversion, upgaze; infraversion, downgaze.

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A

B FIGURE 5-3A,B. (A) Versions showing overaction of the oblique muscles: upper drawing, right inferior oblique overaction 3; lower drawing, right superior oblique overaction 3. (B) Versions showing underaction of the oblique muscles: upper drawing, 3 underaction of the right inferior oblique; lower drawing, 3 underaction of the right superior oblique.

looking around the occluder to see if the eye manifests the oblique dysfunction (Fig. 5-4).

Measuring Ocular Deviation The methods for measuring the angle of strabismus have been divided into the following categories: light reﬂex tests, cover tests, and subjective tests. Light reﬂex tests are the easiest to perform on young children and infants. These tests, however, are not as precise as other tests such as the cover tests. The Lancaster red-green test is useful in adult patients with diplopia and an incomitant deviation. Most methods for measuring ocular deviations involve prisms. There is a basic discussion on the use of prisms in stra-

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FIGURE 5-4. Versions showing an occluder is placed in front of the right eye to ensure that the patient ﬁxates with the left eye. When patient is ﬁxing left eye, it allows the inferior oblique overaction to become obvious and manifest. If the patient were to ﬁx with the right eye, however, one would not see a downshoot because of Hering’s law.

bismus in Chapter 3. For prism neutralization of a deviation, remember to orient the prism so the apex points in the same direction as the deviated eye. Esotropia is corrected with a baseout prism, exotropia with a base-in prism, and hypertropia by a base-down prism. When measuring a deviation, it is critical that the patient is ﬁxating and appropriately accommodating on the ﬁxation target. Accurate measurements cannot be obtained if the patient is gazing around the room or daydreaming and not accommodating on the ﬁxation target. An accommodative target is a target that has ﬁne detail that requires accurate accommodation to be seen. A penlight, for example, is a poor accommodative target as there is no ﬁne detail and accommodation is not required to see the light. One of the best accommodative targets for adults, in the distance or near, is Snellen letters at a size close to visual threshold. By having the patient read the letters, the examiner knows that the patient is accommodating on the ﬁxation target. For young children, small detailed toys or small pictures with ﬁne detail can be used at near and a children’s video or animated toys in the distance.

LIGHT REFLEX TESTS HIRSCHBERG TEST The Hirschberg test, or corneal light reﬂex test, assesses eye alignment by the noting the location of the corneal light reﬂex within the pupil. The term corneal light reﬂex is a misnomer, as it is not a reﬂex off the cornea. What we perceive as the light reﬂex is actually the ﬁrst Purkinje image, which is a virtual

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image located behind the pupil. The Hirschberg test should be performed by holding a light source (muscle light or penlight) in front of the examiner’s eye and directing the light into the patient’s eyes. Have the patient look at the light, then assess the location of the light reﬂex in each eye. Hirschberg testing is only valid if the patient ﬁxes on the light source. The examiner must view the light reﬂexes from a position directly behind the light source. Therefore, for practical purposes, the Hirschberg test can only be performed at near. An accommodative ﬁxation target can be placed next to the light source to attract the patient’s attention and provide an accommodative target. With normal orthotropic alignment, the light reﬂexes are slightly decentered nasally, but they are symmetrically located within each pupil. Slight symmetrical nasal displacement of approximately 5° is normal and is a “physiological” positive angle kappa (see Angle Kappa, below). Patients with strabismus will have an eccentric light reﬂex in the deviated eye. Temporal displacement of the light reﬂex indicates esotropia, nasal displacement indicates exotropia, and inferior displacement indicates hypertropia (Fig. 5-5). One can estimate the size of an ocular deviation by the amount of light reﬂex displacement within the pupil. Temporal displacement of the light reﬂex to the pupillary margin indicates an esotropia of 15° (ET 30 PD), displacement to the temporal midiris indicates esotropia 30° (ET 60 PD), and temporal displacement to the limbus indicates an esotropia of 40° (ET 80 PD). Another way to estimate the angle of deviation is to multiply the millimeters of light displacement by 15 PD to give the deviation in prism diopters.3,6,7 Thus, 2 mm of nasal displacement of the reﬂex from its normal location when viewing monocularly indicates an exotropia of 30 PD. These are relatively gross estimates and, as a rule, are not used to determine the amount of surgery.

ANGLE KAPPA Angle kappa measures the angle between the line of sight and the corneal–pupillary axis. The line of sight is a line from the ﬁxation target to the fovea, and the corneal–pupillary axis is a line from the center of the pupil that is tangential to the cornea. Angle kappa is a monocular measurement of monocular alignment to a visual target. Angle kappa does not have any relationship to the fellow eye and does not measure strabismus. If the fovea is located directly behind the pupil, then the line of sight would be in line with the corneal–pupillary axis and the

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FIGURE 5-5. Hirschberg test: top drawing, normally centered reﬂex; second drawing, esotropia, right eye, with the light reﬂex deviated temporally; third drawing, exotropia, right eye, with the light reﬂex deviated nasally; bottom drawing, right hypertropia, with the light reﬂex deviated inferiorly.

angle kappa would be 0°. On the other hand, a fovea located off center (not directly behind the cornea) creates a discrepancy between the line of sight and the corneal–pupillary axis, resulting in an angle kappa (Fig. 5-6). A positive angle kappa is associated with a temporally displaced fovea (Fig. 5-6A). With the fovea displaced temporally, the eye must abduct to put the image on the fovea, which causes a nasal displacement of the Hirschberg light reﬂex and gives an exo-appearance. Figure 5-7A shows a patient with a positive angle kappa, left eye, caused by a dragged left macula secondary to retinopathy of prematurity. This patient appears to have an exotropia but is actually orthotropic. When the left eye is covered, the right eye remains

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abducted, as this is the position necessary to view the target (Fig. 5-7B). Remember, angle kappa relates to the eye position during monocular viewing and is associated with central ﬁxation by an ectopic fovea. Note that patients with a positive angle kappa and esotropia look as if the eyes are straight. A positive angle kappa can occur congenitally or, if the fovea is dragged temporally, by retinal ﬁbrosis occurring with diseases such as retinopathy of prematurity or a temporal retinal scar from Toxocara canis. A negative angle kappa is caused by nasal displacement of the fovea toward the optic nerve (see Fig. 5-6B); this results in a turning in of the eye, a temporal shift of the Hirschberg light reﬂex, and an eso-appearance. Nasal macular displacement can be secondary to a retinal scar located between the fovea and optic nerve or can occur congenitally without a speciﬁc etiology.

A B FIGURE 5-6A,B. (A) Positive angle kappa. The eye turns out to pick up ﬁxation under monocular viewing conditions as the fovea (F) is displaced temporally. Note that the line of sight differs from the corneal pupillary axis. (B) Negative angle kappa. The eye deviates nasally to pick up ﬁxation as the fovea is displaced nasally, close to the optic nerve. Again, the line of sight is not parallel with the corneal pupillary axis.

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A

B FIGURE 5-7A,B. Clinical photograph of a patient with retinopathy of prematurity. Both foveas are dragged temporally. (A) The patient appears exotropic and both eyes are exotropic, unlike true exotropia where the ﬁxing eye is straight and the nonﬁxing fellow eye is deviated. This patient has a positive angle kappa and is actually fusing with both eyes deviated temporally to align the foveas. (B) There is no ocular shift when the left eye is covered: no exotropia.

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Most normal patients have a physiological positive angle kappa, as the fovea is located 5° temporal to the center of the posterior pole; this is why we usually see the Hirschberg light reﬂex as being slightly decentered nasally in orthotropic patients. An angle kappa can be distinguished from a tropia by the cover/uncover test (see following). If the light reﬂex is displaced from the center of the pupil with monocular viewing, this indicates an abnormal angle kappa, not strabismus (Fig. 5-7B).

KRIMSKY TEST The Krimsky test adds use of a prism to the Hirschberg test to measure a strabismus. This test is indicated to estimate the deviation size in uncooperative patients and patients with sensory strabismus and poor vision of 20/400 or worse. A prism is placed in front of one eye, with the base oriented appropriately (esotropia, base-out; exotropia, base-in; hypertropia, base-down) to neutralize the deviation. A penlight is then shone into both eyes as described for the Hirschberg test. The patient is directed to ﬁxate on an accommodative target juxtaposed to the penlight. The prism is increased or decreased until the reﬂex from each eye becomes equally and symmetrically centered in the pupil. Placing a prism over the ﬁxing eye in a patient with a tropia will cause a version movement in which both eyes move in the direction of the apex of the prism, which moves the light reﬂex in the deviated eye (Fig. 5-8). Placing the prism over the nonﬁxing eye directly moves the light reﬂex to the center of the pupil without a version shift. One can place the prism over either eye, except in cases of a restriction or paresis. In these patients, measure the primary deviation by placing the prism over the eye with limited rotations and mesure the secondary deviation by placing the prism over the eye with full ductions (see primary versus secondary deviation, following).

BRÜCKNER REFLEX TEST The Brückner reﬂex test is performed by using the direct ophthalmoscope to obtain a red reﬂex from both eyes simultaneously. Make sure that the patient is looking at the light during the Brückner test; if the patient looks to peripheral targets, the test is invalid. In patients with strabismus, the Brückner test will show asymmetrical reﬂexes with a brighter reﬂex coming from the deviated eye. There is less pigment in the peripheral retina, so the deviated eye will reﬂect more light. This is a screening test that identiﬁes strabismus and pathology that

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A

B

FIGURE 5-8A,B. The Krimsky test in a patient with esotropia. (A) The light reﬂex is deviated temporally in the esotropic left eye. (B) A base-out prism is presented in front of the right eye, which is ﬁxing. The patient continues to ﬁxate with the right eye, but the right eye turns in to pick up ﬁxation. The left eye, because of Hering’s law, moves temporally. The left eye is now centered and the right eye is turned in; however, the light reﬂex would be centered in both eyes; this is the neutralization point, and the amount of prism needed to achieve the neutralization point measures the angle of deviation.

change the normal red reﬂex including anisometropia, gross retinal pathology, large retinal detachment, and corneal, lenticular, or vitreous opacities (see Chapter 4; Figs. 4-13, 4-14).

COVER TESTS COVER/UNCOVER TEST The cover/uncover test is designed to detect the presence of a tropia in patients who appear to have straight eyes and may be fusing. The idea is to test for a tropia without dissociating an existing phoria. Cover/uncover testing is performed by very brieﬂy covering the eye that is thought to be the ﬁxing eye while observing the eye suspected of deviating for a tropia shifts as the eye picks up ﬁxation. If there is no shift, then perform cover/uncover testing on the opposite eye. If there is no shift of either eye after covering and uncovering each eye, then there is no manifest tropia and the eyes are straight, that is, orthotropia. If brieﬂy covering one eye produces a reﬁxation shift of the fellow eye, then a manifest tropia is present. A nasal to tempo-

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ral reﬁxation movement indicates an esotropia, a temporal to nasal shift indicates an exotropia, and a downward shift indicates a hypertropia (Fig. 5-9). Be sure to have the patient ﬁxate on an accommodative target during testing, as the test is invalid if ﬁxation is uncontrolled and wandering. Cover the ﬁxing eye for 1 to 2 s, just long enough to see if there is a shift of the uncovered eye to midline. The cover/uncover test can be dissociating and can manifest an underlying phoria if the test is performed improperly by covering one eye for several seconds. Prolonged occlusion of one eye will break up fusion, and the patient will manifest a phoria that may erroneously be called a tropia because it is associated with the cover test. Remember to brieﬂy cover one eye for only 1 or

A

B C FIGURE 5-9A–C. Cover/uncover test. (A) Esotropia. Left eye is ﬁxing. When the left eye is covered, the right eye moves out to pick up ﬁxation. This outward movement indicates that the right eye is esotropic. (B) Exotropia. Left eye is ﬁxing. When the left eye is covered, the right eye turns in to pick up ﬁxation. The inward movement indicates that the right eye is exotropic. (C) Right hypertropia. Left eye is ﬁxing. Covering the left eye causes the right eye to come down to pick up ﬁxation. Movement of the right eye indicates a right hypertropia.

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2 s, and to remove the cover for several seconds before covering the fellow eye to allow for reestablishment of fusion. A properly performed cover/uncover test will only identify the tropia without disclosing an underlying phoria. A phoria is detected by alternate cover testing (see discussion that follows).

ALTERNATE COVER TESTING The alternate cover test is used to dissociate binocular fusion to determine the full deviation, including both tropia and phoria. The test is performed by alternately occluding each eye, then observing for a reﬁxation shift of the uncovered eye to midline. It is important to hold the occluder over one eye for several seconds to dissociate fusion, then rapidly move the occluder to the fellow eye making sure one eye is always occluded. The direction of the reﬁxation shifts of the eyes to alternate cover testing is interpreted the same as for cover/uncover testing, described previously and shown in Figure 5-9.

INTERPRETING RESPONSES

TO

COVER TESTS

No shift to alternate cover testing indicates orthophoria. A reﬁxation shift to alternate cover testing indicates a strabismus is present, either a tropia, a phoria, or a tropia with a phoria (monoﬁxation syndrome). Patients with a tropia and no fusion and no phoria will show the same shift on cover test and alternate cover test. Patients with a phoria have straight eyes by Hirschberg light reﬂex, and no reﬁxation shift to cover/uncover testing, but do show a shift to the alternate cover test (Fig. 5-10). Patients with a small-angle strabismus and peripheral fusion (monoﬁxation syndrome) will have both a phoria and a tropia. Monoﬁxators, therefore, demonstrate a small shift to cover/uncover testing and a larger shift to alternate cover testing. Cover/uncover testing discloses the tropia, and alternate cover testing breaks down the phoria to show the full deviation,

FIGURE 5-10A–D. Alternate cover test in a patient with an esophoria. (A) Eyes are straight; however, the patient has a tendency to cross (esophoria), but fusional divergence maintains proper alignment. (B) Left eye is covered, dissociating fusion and allowing the left eye to manifest the esophoria. Note that the left eye turns in under the cover. (C) The cover is quickly shifted from the left eye to the right eye without allowing binocular fusion. Now the left eye moves out as the right eye turns in under the cover. (D) The cover is removed and the right eye moves out by fusional divergence to allow the patient to regain fusion.

A

B

C

D

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TABLE 5-2. Clinical Findings of Phorias, Tropias, and Monoﬁxation.

Orthotropia Phoria Tropia 10 PD Monoﬁxation 10 PD

Corneal light reﬂex

Cover/ uncover

Alternate cover

Fusion

Straight Straight Deviation Small deviation

No shift No shift Shift Small shift

No shift Shift Shift Larger shift

Yes Yes No Yes

tropia plus phoria. Comparing cover/uncover testing to alternate cover testing is a good way to diagnose the monoﬁxation syndrome, even in children who are too young to cooperate with sensory testing. Remember, the presence of a phoria is an indication of binocular fusion. Table 5-2 shows the clinical ﬁndings of phorias, tropias, and monoﬁxation.

PRISM ALTERNATE COVER TEST Prism alternate cover testing determines the amount of prism necessary to neutralize the full deviation tropia and any latent phoria. This is the test used to measure a deviation in anticipation of strabismus surgery. The test is performed by ﬁrst using the alternate cover test to estimate the size of the deviation. A prism is then placed over one eye, oriented appropriately, in an attempt to neutralize the deviation. Alternate cover testing is then performed with the prism in place. If there is a residual reﬁxation shift with the prism in place, the prism is changed (either increased or decreased) to neutralize the deviation (Fig. 5-11). When changing prisms, be sure to always keep one eye covered to maintain binocular dissociation. Also, be sure not to stack prisms of the same orientation (horizontal over horizontal or vertical over vertical) to increase the prism power. It is acceptable to stack horizontal over vertical, but stacking prisms of the same orientation results in underestimation of the angle size.

COMMON CAUSES

FOR

VARIABLE MEASUREMENTS

1. Poor control of accommodation. Solution: use targets that require full accommodation to be seen. Targets with small detail close to visual threshold are the best. 2. Variable working distance (usually at near). Solution: control working distance to 1/3 meter at near, and standardize working distance at distance; this is more critical for near measurements. Have a string measured at 1/3 meter to measure the near working distance.

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3. Tonic fusion not suspended; usually seen in patients with intermittent exotropia and accommodative esotropia. Solution: keep binocular vision dissociated by prolonged occlusion with alternate cover testing. Make sure one eye is always covered when changing prisms (this is why prism bars are helpful). 4. Physiological redress ﬁxation movements; commonly associated with large-angle strabismus. Even when the deviation is neutralized, there is an overshoot of the reﬁxating eye. Solution: move occluder away from the patient’s face to allow peripheral vision of the occluded eye. Also, judge the point of neutralization as the point when redress movement is equal to the reﬁxation movement. Finally, bracket the deviation by intentionally overcorrecting with too much prism, then reduce prism until the best neutralization is achieved. 5. Incomitant deviation (A- or V-patterns and lateral gaze incomitance). Small changes of face turns, head tilts, chin elevation, or chin depressions during the exam will change the deviation measured if the deviation is incomitant. Solution: control the patient’s head position for primary position and cardinal ﬁelds of gaze. Consistent head positioning is critical if reproducible measurements are to be obtained. 6. Poor vision. Solution: patient should wear full optical correction during measurements. Use optotypes or ﬁxation targets that the patient can see. For patients with sensory strabismus and vision of 20/400 or worse, use Krimsky to measure the deviation.

MEASURING

IN THE

CARDINAL POSITIONS

OF

GAZE

There are nine cardinal positions of gaze; however, in most clinical situations,5 measuring the deviation in primary position, upgaze, downgaze, rightgaze, and leftgaze is sufﬁcient (see Fig. 5-2). The positions of gaze are usually measured with the patient ﬁxing on a distance target. Sidegaze measurements are obtained by moving the head up, down, right, left, and then in the oblique axes. Measurement of the deviation in primary position should also be done at near (1/3 m). Measurements in the cardinal positions of gaze are very helpful in identifying and quantifying incomitance.

SIMULTANEOUS PRISM COVER TEST The simultaneous prism cover test is used to measure the tropia component of the monoﬁxation syndrome without dissociating the phoria and is therefore used only in patients with small-

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A

B FIGURE 5-11A–B. Prism alternate cover test to measure esotropia. (A) Left eye is esotropic; right eye ﬁxing. (B) Base-out prism is placed before the deviated left eye, and the retinal image moves closer to fovea, but the deviation is still undercorrected.

angle strabismus. The test is performed by ﬁrst estimating the size of the tropia with corneal light reﬂex testing. A prism, as determined by estimating the size of the tropia, is then presented in front of the nonﬁxing eye (i.e., deviated eye) to neutralize the tropia while the ﬁxing eye is simultaneously covered by an occluder (Fig. 5-12A). If the prism neutralizes the tropia, the deviated eye will stay in its deviated position and there will be no reﬁxation shift. If the deviated eye shows a reﬁxation movement, a residual tropia is present. The prism and occluder are withdrawn from the eyes and, after several seconds, a different prism is presented to the deviated eye while the ﬁxing eye is

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F

20

20 Undercorrected with nasal to temporal shift

C

40

No movement F

F

40 40

40

No shift

D FIGURE 5-11C–D. (C) Alternate cover testing is performed, covering ﬁrst right eye, then left eye. Because the prism undercorrects the deviation, there is an outward shift of the uncovered eye. (D) Larger prism (40 prism diopters, PD) is placed in front of the left eye. Alternate cover testing now reveals there is no shift in eye position, as the deviation is completely neutralized.

simultaneously covered. It is important to allow several seconds to elapse before repeating the test so the patient can regain binocular fusion. This process is repeated until there is no shift of the deviated eye when the ﬁxing eye is covered (Fig. 5-12B–D). In patients with the monoﬁxation syndrome, the amount of tropia can be measured with simultaneous prism cover testing, and the alternate prism cover test can be used to measure the total angle, tropia plus phoria. The notation in the clinic chart

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for a typical monoﬁxator with a small-angle esotropia would read ET 6 PD–E 15 PD.

MEASURING INCOMITANT DEVIATIONS If the deviation is comitant and ductions are full, a prism can be placed in front of either eye or even split between the eyes to measure a deviation. However, when measuring patients with an incomitant deviation secondary to ocular restriction or muscle paresis, one must consider the primary versus the secondary deviation (see Chapter 3, Fig. 3-21). In accordance with Hering’s law, the deviation is larger when the eye with limited ductions is ﬁxing (secondary deviation) than when the eye with full ductions (primary deviation) ﬁxes. When measuring a deviation with prisms, remember that the eye without the prism is considered to be the ﬁxing eye, and the eye looking through the prism is the nonﬁxing eye, regardless of ﬁxation preference or the presence of amblyopia; this is because the eye without the prism must come to primary position to ﬁxate during alternate cover testing. So, to measure the primary deviation, place a prism over the eye with limited ductions and measure the secondary deviation by placing the prism over the good eye (Fig. 5-13). The clinically accepted notation for primary and secondary deviation in Figure 5-13 is Left eye ﬁxing 20 PD (primary deviation) Right eye ﬁxing 40 PD (secondary deviation)

FIGURE 5-12A–D. Simultaneous prism cover test for small-angle esotropia. This test is useful for measuring the tropia in a patient with a tropia and a phoria (monoﬁxation syndrome). (A) Right esotropia with left eye ﬁxing. Estimate the deviation, then present a prism over the deviating eye while simultaneously covering the ﬁxing eye. If the prism is sufﬁcient to neutralize the esotropia, the eye behind the prism (in this case the right eye) does not move. (B) Trying a 5 PD prism; it is too small and the right eye moves out to pick up ﬁxation. (C) A 10 PD prism is now used to neutralize the esotropia. In this case, the prism neutralizes the esotropia. (D) The left eye is covered as the 10 diopter prism is placed in front of the right eye. No shift occurs because the 10 diopter prism neutralizes the 10 prism diopter esotropia.

A

B

C FIGURE 5-13A–C. Primary versus secondary deviation. Top ﬁgure, esotropia secondary to a tight medial rectus muscle. Left, diagram of the primary deviation with the nonrestricted eye (left eye) ﬁxing and a 20 prism diopter prism placed in front of the restricted right eye. With the prism in front of the restricted right eye, the image is on the fovea with the eye resting in esotropic position. Note that the ﬁxing eye is always the eye without the prism, regardless of which eye is actually viewing. The three drawings to the right show the secondary deviation (right eye ﬁxing): (A) A 20 prism diopter prism is placed in front of the left eye. The left eye picks up ﬁxation by adducting, and causes the right eye to abduct because of Hering’s law. (B) The amount of force required to move the unrestricted left eye is minimal, so the right eye gets minimal innervational force. With a 20 prism diopter base-out prism over the left eye, the right eye does not abduct sufﬁciently to place the image on the fovea. (C) A 40 diopter baseout prism causes the left eye to deviate greatly, moving the restricted right eye enough to place the image on the fovea. Secondary deviation equals 40 prism diopters, whereas the primary deviation is 20. Note that, with the prism over the left eye, the restricted right eye must come to primary position to ﬁxate.

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Measuring the Accommodative Convergence to Accommodation (AC/A) Ratio To understand the AC/A ratio, we must review measurements of accommodation and convergence. Accommodation is the increase in lens power to clearly focus at near. The closer the ﬁxation target, the more accommodation is needed to keep the image focused on the retina. Accommodation is measured in diopters. The number of diopters of accommodation needed to focus at a speciﬁc near point is the reciprocal of the ﬁxation distance in meters. For example, if the ﬁxation target is at 1/3 m, then an emmetropic patient has to accommodate 3.00 diopters to put the image in focus, 2.00 diopters at 1/2 m, and 1.00 diopter at 1 m. Note, that a 2.00 hypermetrope without correction would have to accommodate 5.00 diopters at 1/3 m (2.00 diopters for the hypermetropia and 3.00 diopters for near ﬁxation). Convergence keeps the eyes aligned on the approaching targets. Because convergence is linked to accommodation, convergence increases as accommodation increases. Additionally, the farther apart the eyes, the more convergence is required to keep the eyes aligned at near. The amount of convergence needed to keep the eyes aligned on a target at a speciﬁc distance is the reciprocal of the ﬁxation distance in meters times the interpupillary distance in centimeters. For example, if the patient has an interpupillary distance of 50 mm and the target is at 1/3 m, the patient must converge 15 prism diopters to keep ocular alignment on the near target (3 diopters 5 cm). If the interpupillary distance is 40 mm for the same working distance of 1/3 m, the required convergence would be 12 prism diopters.

AC/A RATIO Accommodative convergence to accommodation ratio (AC/A ratio) is the amount of change in convergence for a speciﬁc amount of change in accommodation. A high AC/A ratio means the eyes overconverge for a given amount of accommodation (eso-shift at near), whereas a low AC/A ratio means there is underconvergence per diopter of accommodation (exo-shift at near). Two methods for measuring the AC/A ratio are the heterophoria method and the lens gradient method. These tests are based on changing the patient’s accommodation and then measuring the associated change in convergence. Accommodation is changed by either changing the ﬁxation distance (heterophoria

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method) or by changing the amount of accommodation needed for a speciﬁc ﬁxation distance by introducing various numbers of plus and minus spherical lenses (lens gradient method). A third method that does not actually measure the AC/A ratio but measures the relationsip between the distance and near deviation is the clinical distance–near relationship. The clinical distance–near relationship provides information about the overall change in convergence when one looks from distance to near, including the effects of accommodation and proximal convergence. Most clinicians use either the clinical distance–near relationship method or the lens gradient method to determine the accommodation to convergence relationship. When measuring the AC/A ratio for any of these methods, it is important to use accommodative targets, have the patient wear their full optical correction, use alternate cover testing to measure the deviation, and control the ﬁxation target distance. By convention, 6 m (20 ft) is used for distance and 1/3 m (14 in.) for near. Normal AC/A ratio for the heterophoria method and lens gradient method is 4:1 and 5:1, and ratios of 6:1 or more are considered high. For calculations of the AC/A ratio, esodeviations are represented as positive numbers and exodeviations as negative numbers. Heterophoria Method The heterophoria method compares the distance and near deviation to determine the AC/A ratio. It requires measurement of the distance and near deviation in prism diopters and the interpupillary distance in centimeters. The following formula is used to calculate the AC/A ratio by the heterophoria method, where IPD is interpupillary distance (cm), D is distance deviation (PD), N is near deviation (PD), and D A is diopters of accommodation for near ﬁxation (1/3 m 3 diopters): ND Formula: AC/A IPD DA Example 1. Distance ET 31 Near ET 40 Interpupillary distance 50 mm Nearest target distance 1/3 m 3 D accommodation (40 31) AC/A 5 8 (high AC/A ratio) 3

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LENS GRADIENT METHOD The lens gradient method determines the AC/A ratio by measuring the change in ocular deviation associated with a speciﬁc change in lens-induced accommodation. This test changes accommodation by having the patient view an accommodative target through supplemental plus or minus spherical lens. A plus lens relaxes accommodation so that with less accommodation there is less convergence. A minus lens causes increased accommodation, increased convergence, and an eso-shift. The AC/A ratio is calculated by measuring the deviation at a set distance, with and without supplemental spherical lenses, and dividing the difference by the lens power used. Measurements are usually made in the distance to minimize proximal convergence, and a 3.00 diopter lens is usually used. The formula for the gradient method is AC/A

Deviation without lens Deviation with lens Lens in diopters

Example 1. Deviation without lens ET 40 Deviation with 3.00 lens ET 10 40 10 AC/A 10 (high AC/A ratio) 3 Example 2. Deviation without lens XT 4 Deviation with 3.00 lens ET 14 4 14 AC/A 6 (normal AC/A ratio) 3 Another useful calculation is to estimate the effect of a spectacle lens on a deviation, given an estimated AC/A ratio, as shown in Examples 3 and 4: Example 3. If a child is assumed to have a normal AC/A ratio (5) and an exophoria of 10 PD, what is the effect of changing the patient’s spectacle correction by 2.00 diopters? As the minus 2.00 lens increases accommodation by 2.00 diopters, and convergence is increased by a ratio of 5 to 1 (AC/A ratio 5), the 2.00 lens overcorrection would result in 10 PD of convergence and orthophoria.

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Example 4. A child has a 4.00 refractive error and a 30 PD esotropia. Assuming the AC/A ratio is high normal (6), what will be the effect of the full hypermetropic correction on the deviation? A 4.00 diopter lens will cause 24 PD of divergence; thus, the deviation with glasses will be esotropia of 6 PD. Thus, prescribing the hypermetropic glasses would have a good chance of correcting the deviation with only a small residual deviation.

Clinical Distance–Near Relationship The clinical distance–near relationship does not speciﬁcally measure the accommodative convergence nor is it a ratio. It is a simple comparison of the deviation in the distance to the deviation at near. One can ﬁgure the clinical distance–near relationship by subtracting the distance deviation from the near deviation. A distance–near difference within 10 PD is considered normal whereas differences greater than 10 PD are considered high. This clinical distance–near relationship is a simple, but very useful, method for identifying patients with a high AC/A ratio. N D clinical distance–near relationship D distance deviation viewing target at 6 m (20 ft) N near deviation viewing target at 1/3 m D ET 20 N ET 40 AC/A relationship: 40 20 20 (high AC/A ratio)

Example 1:

D XT 10 N ET 20 AC/A relationship: 20 (10) 30 (high AC/A ratio)

Example 2:

D ortho N XT 15 AC/A relationship: 15 0 15 (low AC/A ratio)

Example 3:

Lancaster Red-Green Test The Lancaster red-green test is a fovea-to-fovea test with two ﬁxation targets, one that the examiner controls and one controlled by the patient. This test is very useful for measuring incomitant strabismus in patients with diplopia and NRC. The

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ﬁxation targets are red- and green-colored linear streaks of light that are projected on a screen. The patient wears red-green glasses (usually red over right eye) and holds one light (green light in Fig. 5-14) while the examiner holds the second light (red light in Fig. 5-14). The examiner projects the red light on the screen, and the patient is directed to look at the red light. Because the patient’s right eye with the red ﬁlter only sees the examiner’s red light, the right eye (fovea) aligns with the examiner’s light. Thus, the right eye becomes the ﬁxing eye and its position is controlled by where the examiner places the red light. Next, the patient is directed to aim the green light (which they are holding) over the examiner’s red light. Because the left eye only sees the green light, the patient moves the green light over the red light by orienting the green light so it falls on the left fovea. The patient now sees the two lights superimposed, as both lights fall on the fovea of each eye. The patient in Figure 5-14 has a left esotropia, so with the green ﬁlter over the left eye, the patient directs the green light to the right of the red light. Patients with orthotropia will place the lights on top of each other, whereas a patient with a left exotropia will point the green light to the left of the red light. The Lancaster red-green test directly shows the examiner where the eyes (foveas) are pointing, which is just the opposite of diplopia tests. The amount of deviation is measured by the amount of separation between the two projected lights on the screen. With the Lancaster red-green test, the eye that sees the examiner’s light is the ﬁxing eye, so the examiner can move the target to various positions on the screen to measure the deviation in eccentric ﬁelds of gaze. Primary versus secondary deviations can be measured by the examiner trading lights with the patient. Torsion can also be assessed in various positions of gaze by observing the tilt of the lines on the screen. Nasal displacement of the top of the line indicates intorsion, and temporal displacement of the top of the line indicates extorsion.

TORSION MADDOX ROD

AND

TORSION

The line seen with the Maddox rod can be used to determine subjective torsion, with a single lens (single Maddox rod test) or a lens over each eye (double Maddox rod test). With the double Maddox rod test, the patient is asked to make the two streaks of the Maddox rod parallel. If the eyes are straight, a prism can

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A B C FIGURE 5-15A–C. Double Maddox rod test with the patient perceiving the streak of light vertically. Remember, this is not a localizing test, and change in torsion is relative to the fellow eye. (A) Normal patient with no torsion. The Maddox rods are aligned at the zero position for each eye. (B) A patient with right incyclotorsion 15°, relative to the left eye, with the right Maddox rod turned clockwise. (C) Patient with bilateral extorsion, 15° each eye. Total extorsion is 30°.

be used to induce a deviation either horizontally or vertically to separate the lines of the Maddox rod. Patients without torsion see parallel lines (Fig. 5-15A), those with intorsion see the 12 o’clock position turned nasally (Fig. 5-15B), and those with extorsion see the 12 o’clock position turned temporally (Fig. 515C). Note that the Maddox rod tests, and most subjective torsion tests for that matter, do not localize the eye with the torsion; they only measure the relative difference in torsion between the two eyes. One often ﬁnds a monocular torsion with the subjective Maddox rod testing but detects bilateral torsion by objective testing with indirect ophthalmoscopy because the eye that the patient perceives to have torsional misalignment depends on which eye is ﬁxing (ocular dominance). To ﬁnd the total torsion with the double Maddox rod, add the torsion of the two eyes together.

TORSIONAL DIPLOPIA

IN

FREE VIEW

Patients with retinal intorsion view the world as being extorted, and retinal extorsion cause objects to be perceived as being intorted. A person with intorsion sees the top of a vertical line tilted temporally, and extorsion will cause the top of a vertical line to appear to be shifted nasally.

FIGURE 5-14. Lancaster red-green test in a patient with normal retinal correspondence (NRC), esotropia, and diplopia; this is a fovea-to-fovea test. The patient ﬁxates on the streak of light projected by the examiner. The patient then directs the other light to align with the examiner’s light. Patient will perceive a single streak of light as each light falls on the corresponding fovea, even though the streaks are separated.

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OBJECTIVE RETINAL TORSION Objective retinal torsion is used to estimate the relationship of the fovea to the optic disc. In normal patients, the fovea is located between the midpoint and the lower border of the optic nerve. Patients with torsion will have a shift in the position of the fovea relative to the optic disc. With extorsion, the fovea is shifted below the inferior border of the optic disc, whereas intorsion shifts the fovea higher than the midpoint of the optic nerve. In actuality, the fovea is the center of vision and the optic nerve actually rotates around the fovea. Remember that the indirect ophthalmoscopic view is inverted, so extorsion is viewed when the fovea is above the upper pole of the disc, and intorsion is viewed when the fovea is below the midpoint of the disc. See Chapter 3 (Fig. 3-14) for an example of objective retinal torsion.

Special Tests for Identifying Restriction and Paresis Tests for identifying restriction and paresis include forced duction testing, generated forced duction testing, and saccadic velocity measurement. Restriction and paresis can coexist, especially in cases of long-standing muscle paralysis such as a longstanding sixth nerve palsy. In these cases, the antagonist of the paretic muscle (i.e., the medial rectus muscle in the case of a sixth nerve palsy) contracts and becomes stiff, thus adding a component of restriction to the paralytic condition.

FORCED-DUCTION TESTING Forced ductions are indicated if there is evidence of restricted ductions. Forced ductions is somewhat invasive, however, but can be performed on most cooperative adults. In patients who are scheduled for surgery, forced ductions are performed at the time of surgery. The technique for rectus muscles is to grasp the eye at the limbus and slightly proptose the eye, then rotate the eye into the ﬁeld of limited ductions. If the eye is inadvertently pushed posteriorly during testing, the rectus muscles will slacken, which may cause the examiner to possibly miss a rectus muscle restriction. When examining awake patients, be sure to ask the patient to look in the direction of the forced ductions to relax the muscle that is being tested. The tightness of oblique muscles can be assessed by a retropulse maneuver called the exaggerated traction test, developed by Guyton.4

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ACTIVE FORCED-GENERATION TEST Active forced-generation testing assesses rectus muscle strength. The eye is anesthetized with a topical anesthetic, and the eye is grasped with forceps at the limbus in the same fashion as forced-duction testing. The patient is asked to look into the ﬁeld of limitation while the eye is held in primary position (Fig. 5-16). This author prefers to use a cotton tip applicator instead of forceps, as forceps can tear the conjunctiva. The examiner feels the force generated by the muscle and compares this with the fellow, nonaffected eye. This test is useful in assessing the amount of muscle function associated with any palsy such as sixth nerve paresis or double elevator palsy.

SACCADIC VELOCITY MEASUREMENT There are various ways to measure saccadic velocities. Clinical estimation is available to all clinicians and is simply the observation of fast eye movements. Fast eye movements can be elicited by having the patient look quickly from side to side or by using an optokinetic nystagmus (OKN) drum. An OKN drum is very useful in young children. Patients with rectus palsies will not be able to generate saccades. Quantitation of eye movements can be made by special equipment such as the electro-oculogram (EOG), which measures the velocity of eye movements. Figure 5-17 shows an EOG tracing of a patient with a sixth nerve paresis. The initial part of the tracing shows a vertical spike indicating adduction movement; however, the end of the tracing shows a mild slope indicating slow abduction. Clinically, if the patient is able to generate a saccadic eye movement in the direction of the eye limitation, then the limitation is restrictive and not secondary to paralysis. Normal saccadic velocity depends on the size of the saccadic eye movement. Large eye movements have higher peak velocities. Normal saccadic velocities range from 200 to 700 degrees per second (°/s).1

RESTRICTION Forced-duction testing is a useful test for identifying restrictions. If the eye can not be easily rotated into the ﬁeld of limited ductions, then a restriction is present. Another sign of restriction is the “dog on a leash” eye movement. A patient with restrictive strabismus and good muscle function will show normal saccadic (fast) eye movements until the eye reaches the

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A

B FIGURE 5-16A,B. Forced-generation test on patient with a right sixth nerve palsy. (A) Patient viewing in primary position with the right eye anesthesized and a dry cotton-tipped applicator placed to the temporal limbus. (B) The patient looks to the right and attempts to abduct the right eye. Pressure by the cotton-tipped applicator pushing the eye nasally, prevents the right eye from moving. The examiner can feel the amount of force exerted by the right lateral rectus through the cotton-tipped applicator. Normally, the applicator could not hold the eye in adduction when the patient is actively abducting.

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FIGURE 5-17. Electro-oculogram of patient with a sixth nerve palsy. Upward arrow on the left indicates adduction. Note that the tracing makes a sharp right upturn, showing normal medial rectus function. On the right is abduction (downward arrow). Note that the curve is gradual, indicating decreased lateral rectus function.

restriction; then the eye stops abruptly. If a patient has limited ductions, yet can generate a saccadic eye movement in the direction of the limitation, restriction instead of paralysis is the cause of the limitation. A restriction also causes eyeball retraction and lid ﬁssure narrowing, as the agonist muscle pulls the eye posteriorly against the restrictive leash. A tight medial rectus muscle will cause lid ﬁssure narrowing on attempted adduction. Increased intraocular pressure can also be a clinical sign of restriction. As the eye rotates against the restriction into abduction for a restricted medial rectus muscle, intraocular pressure measurements will be higher than in primary position or in adduction.

PARESIS The inability for a muscle to generate a saccadic eye movement is an important indication of paresis. Even patients with severe restrictive strabismus will be able to generate a small-amplitude saccade in the direction of the restriction. Patients with a muscle palsy show a slow eye movement as compared to the fellow eye or the affected muscle’s antagonist. In contrast to restriction, which causes lid ﬁssure narrowing, paresis causes lid ﬁssure widening and relative proptosis as the patient looks in the ﬁeld of action of the paretic muscle. A patient with a sixth nerve palsy, for example, will show lid ﬁssure widening on attempted abduction because the medial rectus muscles relaxes on attempted abduction as per Sherrington’s law and, with the lateral rectus paretic, the posterior pressure of the orbital fat pushes the eye forward. The active forced-generation test shows relative weakness of the paretic muscle. One can

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compare agonist and antagonist muscle strength, as well as comparing the muscle strength of fellow eyes, to assess muscle function.

Cycloplegic Refraction Cycloplegic refraction should be performed on every new strabismus patient. The standard regimen is 1 drop of cyclopentolate 1% and neosynephrine 2.5% in each eye, times two, 5 min apart; then, perform the refraction 30 min after the last drop. In patients with dark eyes, the drops should be repeated three times. Patients with blue eyes, or patients with pigment dilution syndrome such as ocular albinism, should receive one set of drops. Remember that mydriasis does not mean cycloplegia. The mydriatic effect comes on sooner and lasts longer than the cycloplegic effect. If the patient shows varying refractive error during retinoscopy, then it is likely that the patient has only partial cycloplegia and requires more drops. In cases of heavily pigmented eyes or in patients with variable refractions, it may be advisable to have the patient return for a 1% atropine refraction. In these patients, atropine should be given to both eyes twice a day for 3 days before the refraction. (See Chapter 3 for details on cycloplegic agents.)

Fundus Examination (Objective Torsion) See Chapter 3 and Figure 3-14 for details on fundus examination.

References 1. Bahill AT, Brockenbrough A, Troost BT. Variability and development of normative data base for saccadic eye movements. Investig Ophthalmol Vis Sci 1981;21:116–125. 2. Biedner et al. Stereopsis testing: at the beginning or the end of orthoptic examination. Binoc Vis Q 1992;7:37–39. 3. De Respinis PA, Naidu E, Brodie SE. Calibration of Hirschberg test photographs under clinical conditions. Ophthalmology 1989;96: 944–949. 4. Guyton DL. Exaggerated traction test for the oblique muscles. Ophthalmology 1981;88:1035. 5. Mitchell PR, Wheeler MB, Parks MM. Kestenbaum surgical procedure of torticollis secondary to congenital nystagmus. J Pediatr Ophthalmol Strabismus 1987;24:87–92.

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6. Paliaga GP. Linear strabismometric methods. Binoc Vis 1992;7:134– 154. 7. Ruttum MS, Shimshak KJ, Chesner M. Photographic measurement of the angle of strabismus. In: Campos EC (ed) Strabismus and ocular motility disorders. Basingstoke: Macmillan, 1990:155–160.

6 Sensory Aspects of Strabismus Kenneth W. Wright

SENSORY ADAPTATIONS Visual neurodevelopment changes in response to abnormal stimulation from a blurred retinal image or strabismus. These changes are referred to as sensory adaptations. The speciﬁc type of sensory adaptation depends on when the abnormal visual stimulation occurred, the severity of the abnormal stimulation, and type of binocular disruption. In Chapter 4, we discussed cortical suppression and amblyopia, which are basic sensory adaptations to a blurred image or strabismus. This chapter provides a list of more speciﬁc sensory adaptations that are encountered clinically. These adaptations are divided into two sections based on the onset of the sensory insult: (1) visually mature and (2) visually immature. A discussion of important sensory tests is provided at the end of this chapter.

MATURE VISUAL SYSTEM The following sensory adaptations occur after the development of bifoveal fusion, when the visual system is mature. Visual development continues until approximately 7 to 8 years of age. After that, there is minimal visual-neurological plasticity. There are some exceptions, however, and prolonged visual plasticity into adulthood has been reported (see discussion at the end of this section: Prolonged Visual Plasticity).

Diplopia Acquired strabismus in patients over 7 or 8 years of age usually results in double vision (i.e., diplopia). Diplopia is also reported 174

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in younger children with acquired strabismus, but it is usually transient and lasts only 2 to 4 weeks before the diplopia is cortically suppressed. The patient with diplopia will ﬁxate on an object with one fovea, and see a diplopic image of that object that comes from the perifoveal retina of the deviated eye (Figs. 6-1, 6-2). The fovea of the deviated eye is suppressed to avoid simultaneously seeing two different objects, one from each fovea (see below: Confusion). Thus, the patient with one eye ﬁxing on

Red Filter

Patient's Perception Uncrossed Diplopia FIGURE 6-1. Esotropia with uncrossed diplopia. The image of the skier falls on the fovea of the left eye and on the nasal retina of the deviated right eye. A red ﬁlter over the right eye causes the diplopic image from the right eye to be red. Note at the bottom of the ﬁgure: the patient perceives the red image from the right eye to be located to the right of the clear image, resulting in uncrossed diplopia.

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Red Filter

Patient's Perception Crossed Diplopia FIGURE 6-2. Exotropia with image falling on the fovea of the left eye and on temporal retina of the right eye, causing crossed diplopia. A red ﬁlter over the deviated right eye causes the diplopic image from the right eye to be red. Note at the bottom of the ﬁgure: the patient perceives the red image from the right eye to be located to the left of the clear image, resulting in crossed diplopia.

a painting and the deviated eye pointed to a lamp will see two paintings, not a painting superimposed on a lamp. The image from the ﬁxing eye will be in clear focus located directly in front of the patient, while the diplopic image from the deviated eye will appear blurred and off center because it comes from the peripheral retina.

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RE

LE

FIGURE 6-3. Patient with a left hypertropia. A red ﬁlter over the deviated left eye causes the diplopic image from the left eye to be red. The X projects to the fovea of the ﬁxing right eye and to the superior retina of the deviated left eye. Because the superior retina views the inferior visual ﬁeld, the red diplopic image in the left eye is seen below the clear image from the right eye.

Esotropia causes the image to fall on the nasal retina of the esotropic eye, which projects temporally and causes uncrossed diplopia because diplopic image is on the same side as the deviated eye (see Fig. 6-1). Exotropia causes the image to fall temporal to the fovea of the exotropic eye, which projects to the nasal ﬁeld, producing crossed diplopia (see Fig. 6-2). We can remember the s in esotropia means same side diplopia (uncrossed), and the x in exotropia means a cross for crossed diplopia. In cases of vertical strabismus, the hypertropic eye perceives the object as being below the image from the ﬁxing eye (Fig. 6-3). Aniseikonia is a difference in image size between eyes and is a cause of diplopia. Aniseikonia is usually caused by anisometropia and is treated with spectacles. An acquired retinal image size disparity up to 7% is usually tolerated, but aniseikonia over 10% may result in diplopia.

Confusion Under rare circumstances, instead of diplopia, patients with acquired strabismus see two different images superimposed on each other, one image from each fovea. If the right eye is looking at a painting and the left eye is pointed at a lamp, the patient with confusion will see the lamp superimposed on the painting. This simultaneous perception from the ﬁxing fovea and the devi-

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ated fovea is termed confusion. Most patients with acquired strabismus do not experience confusion because they suppress the foveal area of the deviated eye and see the diplopic image from the peripheral retina. Confusion is exceedingly rare; however, this author has reported a patient with tunnel vision secondary to glaucoma and acquired strabismus who had confusion rather than diplopia.10 The peripheral visual ﬁeld loss associated with the glaucoma probably forced foveal ﬁxation of the deviated eye. It is likely that suppression of the fovea of the deviated eye is dependent on peripheral retinal stimulation by the diplopic image and, therefore, foveal suppression is not possible when the peripheral ﬁeld is eliminated.

IMMATURE VISUAL SYSTEM Sensory adaptations occur when the binocularity is disrupted by strabismus or a blurred retinal image during the ﬁrst few years of life, usually before 6 years of age. The speciﬁc type of sensory adaptation depends on many factors, including the size of the strabismus, whether it is intermittent or constant, the age of onset of the strabismus, and the age when the strabismus is corrected. Once childhood sensory adaptations are acquired, they are usually present throughout the patient’s life. Cortical suppression is a basic mechanism present in virtually all sensory adaptations to strabismus and a unilateral blurred retinal image. Cortical suppression and amblyopia are discussed in Chapter 4. Herein is a discussion of speciﬁc patterns of suppression and abnormal binocular vision. The following discussion of sensory abnormalities presumes that strabismus is the primary event and that the brain develops sensory adaptations in response to the abnormal visual stimulation. In this author’s view, this is probably true for the majority of strabismus cases; however, strabismus can also occur as a secondary consequence of poor binocular fusion. Examples of a primary fusion deﬁcit and secondary strabismus include sensory strabismus (i.e., unilateral congenital cataract) and central fusion loss associated with closed head trauma. It should be pointed out that some would argue that most types of childhood strabismus are a consequence of congenitally abnormal fusion centers within the brain, not motor misalignment degrading binocular fusion. The answer to this controversy— which came ﬁrst, the strabismus or the sensory fusion abnor-

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mality?—remains unanswered. The fact that one can recover excellent binocular fusion and stereoscopic vision with early and aggressive treatment suggests that, at least in some cases, the sensory abnormality is secondary to the strabismus.

Monoﬁxation Syndrome (Peripheral Fusion) Small-angle strabismus (10 prism diopters, PD) or mild to moderate unilateral retinal image blur in young children and infants causes a suppression of the central visual ﬁeld of the deviated or blurred eye. The small suppression scotoma allows for peripheral fusion (Fig. 6-4). This sensory adaptation, ﬁrst described by Marshall Parks, is termed the “monoﬁxation syndrome.”3 Suppression is localized to within the central 4° to 5° because the central retina has small receptive ﬁelds and high spatial resolution potential; therefore, relatively small differences in image clarity or retinal image position are recognized. In the peripheral ﬁelds, however, slight interocular image differences are not detected, as the peripheral retina has large receptive ﬁelds and relatively low spatial resolution. Thus, small retinal image discrepancies between the eyes are not disruptive in the peripheral ﬁelds, and peripheral fusion occurs. The size of the suppression scotoma is directly proportional to the amount of image blur and size of the strabismus. If the interocular image disparity is too great, even peripheral fusion will be disrupted. Thus, strabismus greater than 10 PD or severe unilateral image blur (e.g., unilateral dense cataract) will disrupt even peripheral fusion. These patients will lack binocular fusion and will not have the monoﬁxation syndrome. Because patients with the monoﬁxation syndrome have motor fusion, they often have a relatively large underlying phoria in addition to a small tropia, giving rise to the term phoria-tropia syndrome. Patients with monoﬁxation syndrome usually have stereoacuity in the range of 3000 to 70 s arc, and the central suppression scotoma measures between 2° and 5°. The Bagolini striated lens test is a sensory test that presents a linear streak of light to each eye oriented 90° apart and centered on the ﬁxation light (Fig. 6-5). Patients with normal binocular vision describe a cross through the center of a ﬁxation light (Fig. 6-5A). In contrast, patients with the monoﬁxation syndrome will describe a cross with a gap in the center of the line presented to the deviated eye (Fig. 6-5B). The gap represents a central suppression scotoma of the nonﬁxing eye. It is impor-

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Small Angle Esotropia Patient's Perception

Suppression Scotoma

A

Anisometropic Amblyopia

Suppression B Scotoma FIGURE 6-4A,B. (A) Diagram of monoﬁxation syndrome secondary to a small-angle esotropia. (B) Hypermetropic anisometropia with amblyopia. In both cases, patient perceives a clear single image, as the suppression scotoma eliminates the discrepancy from the esotropia and blurred image, respectively. Because of the suppression scotoma, the patient sees one clear image.

tant to note that as soon as the dominant ﬁxing eye is occluded, the suppression scotoma vanishes and the patient ﬁxes with the fovea (Fig. 6-5C). The suppression scotoma is often referred to as a facultative scotoma, because its presence is dependent upon ﬁxation with the dominant eye. Worth 4-dot testing is another good method to document the monoﬁxation syndrome. Patients with the monoﬁxation syndrome will fuse the near Worth 4-dot

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A

B

C FIGURE 6-5A–C. Monoﬁxation with microtropia and visual perception with Bagolini lenses. (A) Bagolini lenses over right small-angle esotropia and suppression scotoma, right eye. (B) Retinal images from (A). Note the patient’s perception is one continuous line LE, and one line with an interruption in the center RE. (C) Covering the ﬁxing eye (LE) eliminates the suppression scotoma, and the patient sees a single, continuous line from RE.

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(subtends 6° or 12 PD), but suppress the nondominant eye for the distance Worth 4-dot (subtends 1.25°) because it falls within the suppression scotoma. Further descriptions of these sensory tests follow later in the chapter. Patients with monoﬁxation syndrome often have amblyopia. The amblyopia can be mild (1 or 2 Snellen lines difference) or quite severe (20/200). Even patients with 20/200 amblyopia can still maintain the monoﬁxation syndrome with some peripheral fusion and gross stereopsis. Clinically, the monoﬁxation syndrome is frequently encountered in patients with anisometropic amblyopia, unilateral partial cataract, and small-angle strabismus. Parks described a rare condition, primary monoﬁxation syndrome, which he hypothesized was caused by a congenital lack of central fusion.3

Anomalous Retinal Correspondence Normal retinal correspondence (NRC) is the binocular relationship in which the true anatomic foveas of each eye are functionally linked together in the occipital cortex. Anomalous retinal correspondence, or ARC, is an adaptation to a moderateangle infantile strabismus that allows the brain to accept parafoveal retinal images from the deviated eye and superimposes them with images ﬁxing from the ﬁxing eye. The angle of deviation associated with ARC is usually between 15 and 30 PD, too large to allow peripheral fusion or monoﬁxation. Thus, ARC is a binocular sensory adaptation used to eliminate diplopia by accepting the eccentric image location in the deviated eye as the visual center. This adaptation is a cortical reorganization of retinal correspondence and establishes a new functional fovea called the pseudo-fovea that corresponds to the true fovea of the dominant fellow eye (Fig. 6-6A).8 By cortically establishing a pseudo-fovea at the site of the diplopic image in the deviated eye that corresponds with the true fovea of the ﬁxing eye, the retinal images can be superimposed. ARC and the pseudo-fovea are only present under binocular conditions. When the ﬁxing eye is occluded, the patient changes ﬁxation to the true fovea of the previously deviated eye. If the strabismus of a patient with ARC is partially or fully corrected by surgery or a prism, the image will be displaced off the pseudo-fovea onto the retina that is cortically perceived as being noncorresponding. Because the image is displaced off the pseudo-fovea, the patient will see double even if the image falls

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Patient's Perception

A

B FIGURE 6-6A,B. Anomalous retinal correspondence with right esotropia. (A) Left eye ﬁxes with the fovea (F) and right eye ﬁxes with the pseudofovea (PF). The PF corresponds with the esotropia and is located on the nasal retina. Patient perceives a single image as the pseudo-fovea (PF) of the right eye corresponds with the true fovea (F) of the left eye. (B) Placing a base-out prism to partially neutralize the esotropia. The patient ﬁxes the left eye and sees double, as the image now falls temporal to the pseudo-fovea (PF). Images temporal to the pseudo-fovea (PF) will project to the opposite visual ﬁeld and cause diplopia.

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on the true anatomic fovea. This type of diplopia is called paradoxical diplopia. Remember that under binocular viewing the pseudo-fovea is the central orientation of the eye and images displaced off the pseudo-fovea will be perceived as falling on noncorresponding retina. Figure 6-6A shows a patient with 20 PD esotropia and ARC with a nasal pseudo-fovea, right eye. Note that after partial correction of the esotropia with a 15 PD baseout prism, the image is now temporal to the pseudo-fovea (Fig. 6-6B). This patient will have crossed diplopia because the image falls on retina that is temporal to the pseudo-fovea, and temporal retina projects to the opposite hemiﬁeld. The patient will experience the crossed diplopia so long as the image is temporal to the pseudo-fovea, even if the eyes are aligned so the image falls directly on the true fovea. Adult patients with ARC will often experience some diplopia after correction of their strabismus. An easy way to predict if a strabismic patient has ARC and will have postoperative paradoxical diplopia is to neutralize the angle of deviation with a prism. If the patient has diplopia with prism neutralization of the deviation, then the patient has ARC and the patient should be informed that postoperative diplopia will occur after the eyes are straightened. Fortunately, paradoxical diplopia is usually not so bothersome as true diplopia associated with normal retinal correspondence and, in most cases, paradoxical diplopia will vanish within a few weeks after surgery. Only in rare circumstances is postoperative paradoxical diplopia so bothersome that it interferes with everyday activities. Even so, in rare instances, persistent postoperative paradoxical diplopia has required a reoperation to recreate the initial strabismus to eliminate paradoxical diplopia. In cases where preoperative prism neutralization creates paradoxical diplopia that bothers the patient, one can prescribe press-on prisms (prism adaptation) to see if the diplopia will subside over several weeks. Bagolini striated lenses on a patient with a 20 PD esotropia and ARC are depicted in Figure 6-7A. The patient perceives a cross (normal response) even though there is an esotropia, because the line in the deviated eye passes through the pseudofovea. If a strabismic patient reports seeing a complete cross to Bagolini striated lenses, then they have ARC (Fig. 6-7B). This cortical reorganization of ARC is only present during binocular viewing and, when the dominant eye is covered, the patient reorients to the true anatomic fovea (Fig. 6-7C). ARC should not be confused with eccentric ﬁxation. Remember, ARC is only

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A

B

C FIGURE 6-7A–C. Anomalous retinal correspondence (ARC) as tested with Bagolini lenses. (A) Bagolini lenses stimulate the right fovea (F) and left pseudo-fovea (PF). Note that the pseudo-fovea (PF) is nasal to the true fovea (F). (B) Retinal location of the Bagolini striation when the fovea (F) of the right eye is being stimulated and the pseudo-fovea (PF) of the left eye is being stimulated. Patient’s perception is a cross, as the pseudo-fovea (PF) corresponds to the true fovea (F). (C) When the right eye is occluded, the patient now ﬁxates with the true fovea (F) of the left eye. Note that the pseudo-fovea has disappeared. Patient perceives a single line, which stimulates the visual center.

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present during binocular viewing, whereas eccentric ﬁxation represents a monocular loss of vision (amblyopia) and is present during both monocular and binocular viewing. ARC provides crude binocular vision with superimposition of retinal images; however, there is not true fusion. Patients with ARC do not have fusional vergence amplitudes, and they do not have stereoacuity. ARC can occur in association with intermittent strabismus. Some patients with intermittent exotropia, for example, have binocular vision with stereopsis when they are aligned but switch to ARC when they are tropic. In general, ARC is associated with good vision or only mild amblyopia. Harmonious ARC is the term used for the situation as described previously where the position of the pseudo-fovea completely compensates for the angle of strabismus (see Fig. 66). Described another way, the strabismic deviation equals the pseudo-foveal offset from the true fovea. The amount of pseudofoveal offset is termed the angle of anomaly, which is equal to the strabismic deviation (objective angle). Clinically, however, there are many cases in which the angle of strabismus does not exactly match the location of the pseudo-fovea so that the target image does not fall on the pseudo-fovea. This condition is called unharmonious ARC. In Figure 6-8A, the angle of the strabismus measures 20 PD (objective angle), but the pseudo-fovea is only 15 PD from the true fovea (angle of anomaly 15 PD). Thus, the image is falling 5 PD nasal to the pseudo-fovea. A 5 PD base-out prism over the right eye places the image on the pseudo-fovea and eliminates the diplopia. The discrepancy between the location of the pseudo-fovea and the location of the target image is called the subjective angle; in Figure 6-8B, the subjective angle is 5 PD. Note that neutralizing the subjective angle eliminates diplopia associated with unharmonious ARC, but neutralizing more than the subjective angle results in paradoxical diplopia (Fig. 6-8C). In these cases of unharmonious ARC, it is likely that the angle of strabismus has changed (usually increased) after the development of the pseudo-fovea. Most patients with unharmonious ARC suppress the target image so as not to experience diplopia. Others, perhaps those who had a change in the deviation off the pseudo-fovea in late childhood or adulthood, do experience diplopia. Further discussion of unharmonious ARC and angle of anomaly is located under Amblyoscope, later in this chapter.

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A

B

C FIGURE 6-8A–C. Unharmonious ARC in a patient with esotropia. The pseudo-fovea (PF) is not in alignment with the retinal image in the deviated eye. (A) Patient perceives uncrossed diplopia or suppresses the image in the deviated eye. (B) A base-out prism is used to place the image on the pseudo-fovea (PF). Patient perceives a superimposed single image. A red ﬁlter in front of the right eye causes the image to appear pink, a combination of the clear image (left eye) and the red image (right eye). (C) A 20 PD prism is placed base-out in front of the deviated eye to place the image on the true fovea (F). Patient now has paradoxical diplopia and sees the red image on the contralateral side, causing crossed diplopia.

Practically speaking, the differentiation between harmonious versus unharmonious ARC is not of great clinical importance; however, paradoxical diplopia after strabismus surgery is of clinical concern. Adult patients with long-standing strabis-

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mus should be examined for ARC by neutralizing the deviation with a prism.

Large Regional Suppression Children who have large-angle strabismus or severe unilateral retinal image blur develop a large suppression scotoma to eliminate the image disparity (Fig. 6-9). Patients with large-angle constant strabismus (e.g., congenital esotropia), will have essentially no binocularity, not even peripheral fusion or ARC. Large regional suppression, however, is not always constant and can be intermittent. Patients with large-angle strabismus and large fusional vergence amplitudes (e.g., intermittent exotropia) have intermittent strabismus and intermittent regional suppression. These patients switch from a state of binocular fusion to monocular vision and suppression. Another example of intermittent large regional suppression is seen in patients with congenital incomitant strabismus, where the eyes are straight in one ﬁeld of gaze (Duane’s syndrome, or congenital superior oblique palsy). These patients have binocular fusion when their eyes are aligned with a compensatory face turn, but they suppress when they look into the ﬁeld of gaze where they have strabismus. Patients with intermittent exotropia and Duane’s syndrome that have developed suppression do not have diplopia when they are tropic.

Horror Fusionis Normal sensory and motor fusion, once established, is usually permanent. Binocular fusion, however, can be lost if severe and sustained abnormal visual stimulation is acquired. Long-term occlusion of one eye, especially if it is the dominant eye, can result in a loss of binocular fusion in some patients. If this loss of binocular fusion occurs late in visual development or adulthood, the patient will be too old to suppress. The inability to either fuse or suppress images results in intractable diplopia and is termed horror fusionis, or acquired disruption of central fusion. Causes of this rare syndrome include a unilateral acquired cataract occurring in older children and adults.2,4,6 In these cases, prolonged occlusion caused by a cataract appears to eliminate binocular fusion and, if the child is too old to suppress, diplopia results. An acquired cataract in the dominant eye of an adult with previous strabismus or amblyopia can also cause

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FIGURE 6-9. Worth 4-dot in a patient with large regional suppression of the right eye. The two dots fall within the suppression scotoma, so the patient perceives three dots from the left eye.

horror fusionis. In these cases, prolonged occlusion of the dominant eye results in loss of preexisting suppression, leaving the patient with diplopia. In addition, horror fusionis can be caused by antisuppression therapy, such as forcing ﬁxation with the nondominant eye in patients with strabismus. Antisuppression consists of training the strabismic patient to recognize the diplopia, which can be done by using dense red ﬁlters over the dominant eye to force ﬁxation to the nondominant eye. Anti-

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suppression is especially dangerous in patients with strabismus and poor fusion potential.

Prolonged Visual Plasticity The dogma regarding the relatively short span of visual central nervous system plasticity has come into question. Veteran strabismologists know that some adult patients with acquired strabismus can eventually learn to ignore or suppress their double vision. Do these patients actually develop suppression or do they consciously ignore their diplopia? In a study of acquired strabismus in adults, this author used the pattern visual evoked potential (VEP) to document suppression of visual cortical activity in adult patients with acquired strabismus.10 Another example of prolonged plasticity is seen in adults with amblyopia, who can show signiﬁcant visual acuity improvement after losing vision in their good eye.1,7

Sensory Tests DIPLOPIA TESTS Diplopia tests use one ﬁxation target seen by both eyes. The target images fall on both foveas and corresponding retinal points if the eyes are aligned (Fig. 6-10). If strabismus is present, the target image falls on the fovea of the ﬁxing eye and an extrafoveal point in the nonﬁxing eye (Fig. 6-11). A color ﬁlter is placed over one eye (usually red) or both eyes (usually red for right eye, green for left eye) to tint the image of each eye. By distinctly tinting the retinal images of each eye, the examiner can tell which image corresponds to which eye. Lenses that place a streak of light on the retina (Maddox rod and Bagolini lens) are also used to stimulate the retina. Many diplopia tests disrupt fusion by obscuring, or even eliminating, peripheral fusion clues. Tests that disrupt fusion are referred to as dissociating tests. Table 6-1 lists different diplopia tests, with the most dissociating test listed ﬁrst and the least dissociating test last. Note that under scotopic conditions tests that use ﬁlters, such as the Worth 4-dot test and red ﬁlter test, become extremely dissociating, because the only images seen by the patient are the test lights and peripheral fusion clues are lost.

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Red Filter Test Othotropia NRC

Penlight

RE

LE

F

F

L

Center

R Binocular Perception

One Pink Light FIGURE 6-10. Red ﬁlter test in a normal patient with straight eye and normal retinal correspondence. Note that the image from the penlight falls on both foveas and the patient perceives a single binocular image.

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Red Filter Test R-Esotropia ARC

Penlight

LE

RE

F F

P

L

Center

R Binocular Perception

One Pink Light FIGURE 6-11. Red ﬁlter test in a patient with a right esotropia and ARC. Red ﬁlter is placed in front of the right eye (RE) and the image falls on the pseudo-fovea (P) and fovea, representing corresponding retinal points in a patient with ARC. The patient has a single binocular perception and sees one pink light. LE, left eye.

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TABLE 6-1. Types of Diplopia Tests. Most dissociating Maddox rod Dark red ﬁlter Worth 4-dot with room lights out Worth 4-dot with room lights on Least dissociating Bagolini striated lenses

SPECIFIC DIPLOPIA TESTS RED FILTER TEST One of the simplest diplopia tests is the red ﬁlter test. Place a red glass over one eye and direct the patient to ﬁxate on a single light source, or an accommodative ﬁxation target. Patients with straight eyes and normal retinal correspondence will see one pinkish-red light (see Fig. 6-10). If a phoria is present, the red ﬁlter may dissociate the eyes and then the patient will manifest their deviation and see double. The denser the red color, the more dissociating the test. Another way to make the standard red ﬁlter test more dissociating is to turn down the room lights. In dim illumination, the eye behind the red ﬁlter will only see the light source, not background objects in the room, which will eliminate peripheral fusion clues. The red ﬁlter test is useful for identifying NRC, ARC, and suppression. Esotropia with NRC causes uncrossed diplopia, with the red light seen on the same side as the red ﬁlter (see Fig. 6-1). Alternately, exotropia with NRC is associated with crossed diplopia as the red light is opposite to the red ﬁlter (see Fig. 6-2). When the deviation is neutralized with a prism, the diplopia disappears and the images will be superimposed. Patients with ARC will generally see one light, even though they have strabismus, because they use a pseudo-fovea. In Figure 6-11, the red light falls on the pseudo-fovea of the right eye. This image is cortically superimposed with the foveal image of the left eye to produce the perception of one pink light. If partial or full prism neutralization of the deviation results in diplopia, then the patient has ARC. Strabismus associated with suppression results in the perception of a single light, either a red or a white light, depending on which eye is ﬁxing. In Figure 6-12, the left eye is ﬁxing, so the patient sees one white light and suppresses the red light falling on the right retina. If a dark red ﬁlter is placed over the

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Red Filter Test (Esotropia and Suppression RE) NRC

Penlight

Red Filter

LE

RE

F F Suppression Scotoma L

Center

R Binocular Perception

LE One White Light

FIGURE 6-12. Red ﬁlter test in a patient with childhood esotropia who developed suppression and a ﬁxation preference for the left eye. Patient ﬁxes left eye with a suppression scotoma of the right eye. Note that the retinal image of the penlight falls within the suppression scotoma, so the patient only perceives one white light from the left eye.

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ﬁxing left eye, then ﬁxation switches to the right eye, and the left eye is suppressed (Fig. 6-13). Patients who alternate ﬁxation may report seeing two lights: a red light alternating with a white light. When a child with a manifest strabismus claims to see two

Red filter over LE

Penlight

Dark red filter

LE

RE

F

F

Suppression Scotoma L

Center

R Binocular Perception

RE One White Light FIGURE 6-13. A dark red ﬁlter is placed over the left eye to shift ﬁxation to the right eye. With the right eye ﬁxing, patient suppresses the image in the left eye and perceives one white light from the right eye.

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lights, be sure to distinguish between diplopia, where the red and white lights are seen simultaneously, and alternating suppression, where one light is seen at a time. Partial or full prism neutralization of the strabismus will not result in diplopia. The patient with suppression will continue to see just one light.

VERTICAL PRISM RED FILTER TEST/SUPPRESSION VERSUS ARC Another way ARC can be distinguished from NRC in patients with suppression is by placing a red vertical prism (usually 15 PD base-down) over the deviated eye. A vertical prism causes patients with ARC to see two vertically displaced images, with the red light directly over the white light (Fig. 6-14). The lights are vertically aligned because the light in the deviated eye is over the pseudo-fovea that corresponds to the true fovea of the ﬁxing eye. When a vertical prism is introduced to the deviated eye of a patient with central suppression and NRC, the patient reports seeing two lights that are horizontally and vertically displaced because there is no pseudo-fovea and the center of reference is the true fovea of each eye (Fig. 6-15).

WORTH 4-DOT The Worth 4-dot test consists of two green lights, one red light, and one white light (Fig. 6-16). The patient wears red/green glasses, usually with the red lens over the right eye, and views a Worth 4-dot ﬂashlight at one-third of a meter, or a Worth 4dot light box at 6 m (20 ft). The near Worth 4-dots are separated by 6° at near (ﬂashlight at 1/3 m) and by 1.25° for the distance (light box at 6 m). When the test is performed with the room lights out, the white dot is the only binocular fusion target, as it is the only light seen by both eyes. Green lights are seen through the eye behind the green ﬁlter, and the red light is seen with the eye with the red ﬁlter. If the room lights are turned on, however, the patient can see the room environment with both eyes, including the Worth ﬂashlight and examiner, thus providing strong fusion clues; this is why Worth 4-dot testing in the dark is much more dissociating than testing with the room lights on. The normal fusion response is seeing four lights, two red and two green. Another normal response is one red light, two green lights and one light that ﬂickers between red and green. The light that ﬂickers is the white light that is seen by both

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Esotropia ARC

Penlight

RE

L-ET

F

P F

F

Red prism base down L

Center

R Binocular Perception

Vertical Diplopia with two lights in horizontal alignment FIGURE 6-14. Patient with esotropia and ARC is presented with a basedown vertical prism and a red ﬁlter over the left eye. The prism deﬂects the retinal image below the pseudo-fovea (P) and the patient perceives two images: vertically, one on top of the other. Remember, the pseudofovea (P) is the center of vision during binocular viewing.

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Esotropia NRC Suppression

Penlight

L-ET

RE

ET F F

F

Red prism base down L

Center

R Binocular Perception

Vertical and Uncrossed Diplopia FIGURE 6-15. Patient with esotropia and suppression of left eye. A basedown prism is placed in front of the left eye, which displaces the retinal image inferiorly and out of the central scotoma. The patient perceives two images: vertically and horizontally displaced. Note that there is no pseudo-fovea (F) and the true foveas are at the center of vision.

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FIGURE 6-16. Worth 4-dot test in a normal patient with straight eyes. Three lights are projected to the left eye and two lights to the right eye. Patient fuses the two images and perceives four lights.

eyes, the ﬂicker being color rivalry. Patients with acquired strabismus and diplopia will see ﬁve lights: three green and two red. Patients with cortical suppression report seeing either three green lights or two red lights, depending on which eye is ﬁxing. In Figure 6-9, the left eye is ﬁxing and the right eye is suppressed so the patient sees three green lights. If the right eye was the preferred eye and the left eye was suppressed, then the patient would see two red lights. Patients who alternate ﬁxation usually describe seeing two red lights, alternating with three green

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lights. A few patients, however, will report the sum total of the alternating lights, that is, ﬁve lights. Thus, alternating suppression can be confused with diplopia, because patients with diplopia also report seeing ﬁve lights. Patients with large scotomas (scotomas greater than 6°) will suppress both the distance (central ﬁeld) and near (peripheral ﬁeld) Worth 4-dot. Patients with the monoﬁxation syndrome have a small central suppression scotoma (5°) and peripheral fusion. They fuse, or see, four lights for the near Worth 4-dot (which subtends 6°) because the dots fall outside the scotoma (Fig. 6-17), but sup-

FIGURE 6-17. Near Worth 4-dot test in a patient with monoﬁxation syndrome and 8 PD (4°) esotropia. The near Worth 4-dot subtends 6° and the dots fall outside the scotoma. Patient perceives four dots.

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FIGURE 6-18. Distance Worth 4-dot test in a patient with monoﬁxation syndrome and esotropia of 8 prism diopters. The distance Worth 4-dot subtends 1.25° and two dots fall within the central suppression scotoma. Therefore, patient perceives three dots from the left eye and no dots from the right eye.

press the distance Worth 4-dot (which subtends only 1.25°) as the dots fall within the scotoma (Fig. 6-18). One of the best uses of the Worth 4-dot test is to identify the monoﬁxation syndrome (i.e., central suppression and peripheral fusion) in a patient with a small-angle strabismus. The results of this test will tell the examiner if there is peripheral fusion that can be present even if there is no discernible stereoscopic vision. Remember, it is important to leave the room lights on when performing the Worth 4-dot test if the goal is to promote fusion.

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With the room lights on, the patient can see background objects in the room with both eyes, providing binocular peripheral fusion clues. If the lights are dimmed or turned off, however, only the Worth lights can be seen and the only target seen by both eyes is the single white dot. Because of the lack of peripheral fusion clues, the Worth 4-dot test becomes extremely dissociating in the dark. Once one realizes the dissociating power of the dark, one can use this phenomenon to estimate how well a patient fuses. If a patient can maintain fusion of the Worth 4dot test with lights out, then this indicates strong motor fusion. On the other hand, if dimming the lights changes the response from fusion to suppression or diplopia, this reveals relatively weak motor fusion. Patients with intermittent exotropia who have weak motor fusion manifest their deviation when the lights are dimmed. The Worth 4-dot ﬂashlight can be used to plot the size of suppression scotomas. By moving the ﬂashlight closer to the patient, the lights subtend a larger angle (i.e., stimulate more peripheral retina) and by moving the ﬂashlight farther away, the lights subtend a smaller angle (i.e., stimulate more central retina). Table 6-2 describes the stimulus angle for the Worth 4dot ﬂashlight at various distances from the patient.

BAGOLINI LENSES Bagolini striated lenses are clear with a linear scratch through the center of each lens that provides a streak of light on the retina when viewing a bright light (see Fig. 6-5). One lens is placed over each eye, and the lenses are oriented obliquely at 45° and 135°. Because the lenses are otherwise clear, they are not dissociating. Bagolini lenses, therefore, have the advantage of providing a free binocular view without dissociation. Patients with straight eyes and NRC, and those with harmonious ARC, will report seeing a cross (Fig. 6-19A). Remember, with ARC, one line is on the true fovea and the other line falls on the

TABLE 6-2. Stimulus Angle for Worth 4-Dot Flashlight. Flashlight distance from patient 1/6 m 1/3 m (14 in.) 1/2 m 1m a

Standard near Worth 4-dot.

Worth 4-dot angle 12° 6°a 4° 2°

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FIGURE 6-19A–E. Patient perception of Bagolini testing. (A) A cross is perceived in orthotropia with normal retinal correspondence or strabismus with ARC. (B) Patient with strabismus and large suppression scotoma sees one line. (C) Patient with monoﬁxation syndrome and small central scotoma will see one continuous line and one line broken in the center that corresponds to the eye with the suppression scotoma. (D) Patient with esotropia and uncrossed diplopia reports a “V” conﬁguration. (E) Patient with exotropia and crossed diplopia reports an “A” conﬁguration.

pseudo-fovea (see Fig. 6-7). Patients who have large regional suppression will report seeing only one line (Fig. 6-19B). The monoﬁxation syndrome, on the other hand, is associated with a cross, but one line will have a central gap (Figs. 6-19C, 6-5). Patients with NRC, heterophoria, and diplopia will show the response of either an “A” or a “V.” Because esotropia is associated with uncrossed diplopia, esotropia will cause the right line to move to the right and the left line to move to the left, creating a “V” (Fig. 6-19D). Exotropia produces an “A” because exotropia is associated with crossed diplopia, with the right line moving to the left and the left line moving to the right (Fig. 6-19E).

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MADDOX ROD TEST The Maddox rod can be used for identifying horizontal, vertical, and, especially, torsional deviations. The Maddox rod has a washboard appearance as it is made up of multiple cylindrical high plus lenses stacked on top of each other. When the patient views a light through the Maddox rod, a linear streak of light oriented 90° to the cylindrical ribs of the Maddox rod is seen. The single Maddox rod test is performed by placing the Maddox rod over one eye and having the patient view a penlight. The Maddox rod is aligned so the streak is vertical to detect horizontal deviations and then horizontal for vertical deviations. If the streak of light passes through the penlight, the patient is orthophoric, or has harmonious ARC. This is one of the most dissociating tests, because the images to each eye are totally different and there are essentially no binocular fusion clues. The Maddox rod test is so dissociating that it will cause patients with normal bifoveal fusion to manifest their phoria. Because of this, the Maddox rod test, and dissociating tests in general, do not distinguish between phorias and tropias. To make the diagnosis of phoria versus tropia, one must assess the eye alignment objectively before administering the dissociating diplopia test. The Maddox rod test can also be used to measure torsion (as described in Chapter 5).

Haploscopic Tests In contrast to diplopia tests where there is one stationary ﬁxation target that is viewed by both eyes, haploscopic tests have two ﬁxation targets, one for each eye, and the targets can be moved separately to align with each fovea. A haploscopic presentation means each eye receives its own visual stimulus. There are various ways to separately stimulate each eye. One way to create haploscopic vision is to place a mirror in front of each eye, with the mirrors angled so the right eye sees the right temporal side and the left eye sees the left temporal side. Mirror separation of vision is the principle of the amblyoscope. Another commonly used method is to give the patient color-tinted glasses with one eye receiving a red ﬁlter and the fellow eye a green ﬁlter. Two movable targets are presented on a white screen: one red and one green. The eye with the red ﬁlter sees only the red target and the eye with the green ﬁlter sees only the green target; thus, separate visual stimuli are presented to each eye; this is the principle of the Lancaster red/green test. If

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strabismus is present, either the mirrors can be angled or the red/green targets moved so the ﬁxation target is aligned with each fovea. Haploscopic tests include the Lancaster Red/Green Test and the amblyoscope. The Lancaster Red/Green test is used to measure the angle of strabismus (see Chapter 5; Fig. 5-14). Note that the Worth 4-dot test is partially haploscopic because some of the objects in the visual ﬁeld are seen by both eyes. The Worth 4-dot test is not a true haploscopic test, as targets are not independently movable to each eye and cannot be aligned with each fovea.

AMBLYOSCOPE The amblyoscope provides a haploscopic view, allowing presentation of images to each eye independently. Two mirrors at the elbow of the amblyoscope arms reﬂect images from transparent picture slides into each eye (Fig. 6-20). The arms can be moved to measure either subjective or objective angle. The subjective angle is the amount in degrees the examiner must move the amblyoscope arms to allow the patient to see the two pictures

FIGURE 6-20. Amblyoscope testing a patient with normal retinal correspondence (NRC) and orthotropia. A dot is a target for the left eye and a ring is the target for the right eye. Patient sees the dot inside the ring without moving the arms of the amblyoscope.

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as being superimposed. The objective angle is measured by alternating the target presentation from right eye to left eye, moving the arms of the amblyoscope until there is no reﬁxation eye movement. The objective angle equals the deviation as measured by the alternate prism cover test. The subjective angle is determined under binocular viewing conditions whereas the objective angle is measured during monocular viewing.

NORMAL RETINAL CORRESPONDENCE In a strabismic patient with NRC and diplopia, the subjective and objective angles are the same (Fig. 6-21) because patients with NRC always use the fovea as the center of reference. Patients with NRC and dense large regional suppression will not have a measurable subjective angle because they suppress one eye, making subjective superimposition of the images impossible. The subjective angle can be measured in patients with the monoﬁxation syndrome and a small central suppression scotoma by using targets that stimulate the peripheral retina.

FIGURE 6-21. Patient with NRC and esotropia. The arms of the amblyoscope are angled so the image falls on each fovea and the patient perceives the dot inside the circle. Each arm is moved 20 (10°) for a total of 40 .

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FIGURE 6-22. Patient with harmonious ARC and right esotropia. The arms of the amblyoscope do not have to be angled for the patient to see the dot inside the ring, as the pseudo-fovea (P) is directly aligned with the ring target. The patient perceives the dot in the center of the circle with the arms of the amblyoscope parallel aligned to zero.

ANOMALOUS RETINAL CORRESPONDENCE (HARMONIOUS) Patients with strabismus and harmonious ARC have a signiﬁcant objective angle, but the subjective angle is zero. The subjective angle is zero (or close to zero) because the subjective angle is measured under binocular conditions and reﬂects the alignment based on the relationship between the true fovea of the ﬁxing eye and the pseudo-fovea of the deviated eye. Because patients with harmonious ARC have the pseudo-fovea positioned to compensate for the angle of deviation, there is no subjective misalignment. Patients with harmonious ARC will see the targets from each eye as superimposed with the amblyoscope arms set to zero (parallel) even though there is a large objective angle (Fig. 6-22). The objective angle is measured by alternate cover testing, blocking the vision of each eye (monocular viewing) so the objective angle reﬂects the misalignment based on the true fovea. The displacement of the pseudo-fovea off the true fovea is called the angle of anomaly. Because the location

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of the pseudo-fovea completely compensates for the objective deviation in harmonious ARC, the subjective angle is zero, and the objective angle equals the angle of anomaly. For example, in Figure 6-22, the objective angle is ET 20 PD and the subjective angle is zero. The angle of anomaly (i.e., distance of the pseudofovea from the true fovea) is 20 PD (200). In patients with unharmonious ARC, the pseudo-fovea is located in a position that does not fully compensate for the objective deviation. These patients will see double or will suppress the image that does not fall on the pseudo-fovea (Fig. 6-23: “I” image in right eye). The subjective angle is measured by moving the arms of the amblyoscope until the two images are superimposed. When the images are superimposed, the image of

FIGURE 6-23. Patient with unharmonious ARC and 30 PD of esotropia. The arms of the amblyoscope are set at zero and are not angled. As the image (I) is falling nasal to the pseudo-fovea (P), the patient perceives uncrossed diplopia (as diagrammed in the rectangle at the bottom of the ﬁgure). If the arm of the amblyoscope in front of the right eye was moved 10° in to place the image on the pseudo-fovea (P), the patient would perceive the ring around the dot.

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the ﬁxing eye is on the true fovea, and the image in the nonﬁxing eye is on the pseudo-fovea. The subjective angle is the number of degrees from the zero position the amblyoscope arm needs to move to place the image on the pseudo-fovea. For example, in Figure 6-23, the subjective angle (I-P, right eye) is 10 PD, and the objective angle (I-F, right eye) is 30 PD. Because the angle of anomaly (P-F) is equal to the objective angle minus the subjective angle, the angle of anomaly is 20 PD (3010). The amblyoscope is a useful tool as it can measure fusional vergence amplitudes, angle of deviation, area of suppression, retinal correspondence, and even torsion. Some degree of instrument convergence, however, is usually present when using the amblyoscope.

AFTERIMAGE TEST The afterimage test is a fovea-to-fovea sensory test that does not use a haploscopic apparatus, but each eye is stimulated separately. Each fovea is marked individually during monocular viewing with a linear strobe light that bleaches the retina; this causes a linear afterimage shadow through the true fovea that lasts approximately 10 s. The center of the linear strobe light is masked to spare the fovea; thus, the afterimage line has a break in the middle. Testing is performed by having the patient occlude one eye while the other eye ﬁxates on the central masked part of the strobe light held vertically in front of the patient (Fig. 6-24). The ﬁxing eye is stimulated to produce a vertical afterimage. Next, the fellow eye is stimulated with a horizontally oriented strobe light while the ﬁrst eye is covered (Fig. 6-24B). The occluder is quickly removed, and the patient is asked where they see the afterimage lines while they are binocularly viewing (Fig. 6-24C). Because the stimulus is presented under monocular conditions, the stimulus always marks the true fovea of each eye unless there is eccentric ﬁxation from dense amblyopia. Patients with NRC will, therefore, always see a cross whether they are orthophoric, esotropic, exotropic, or hypertropic because their center of reference is the fovea under monocular or binocular conditions (Fig. 6-25A,B). Patients with ARC however, use their true fovea during monocular viewing but, during binocular viewing, the deviated eye switches to the pseudo-fovea. Consequently, patients with ARC have each fovea marked by the monocular afterimage, but when binocular vision is reestablished, the pseudo-fovea takes over as the center of

A

B

C

A

B

C D FIGURE 6-25A–D. Perception of afterimage test in patients with (A) NRC orthotropia, (B) NRC and strabismus, (C) ARC esotropia, and (D) ARC exotropia. Note that the stimulation for the afterimage test occurs under monocular conditions and that the light always tags the fovea, even in patients with ARC. After the stimulation, the patient is again given binocular vision, so the patient switches back to the pseudo-fovea and the image tagged on the fovea appears to be in an eccentric location (C and D).

FIGURE 6-24A–C. Afterimage test of a patient with NRC. If the patient has NRC, the results of the afterimage test are the same whether the patient has straight eyes, esotropia (ET), exotropia (XT), or a hyperdeviation. (A) Right eye is stimulated with a vertical strobe while the left eye is covered. (B) Left eye is stimulated with a horizontal strobe light while the right eye is covered. (C) The cover is removed and the patient reports seeing a cross.

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reference for the deviated eye. As the pseudo-fovea is the center of reference, the afterimage marked on the true fovea is perceived as coming from the peripheral visual ﬁeld. With esotropia, the fovea is temporal to the pseudo-fovea and temporal retina projects to the opposite hemiﬁeld, so the right afterimage is seen on the left (Fig. 6-25C). Exotropia is just the opposite, with the fovea nasal to the pseudo-fovea and nasal retina projecting to the ipsilateral hemiﬁeld, so the right afterimage is seen on the right (Fig. 6-25D).

Other Tests for Suppression and Fusion VECTOGRAPHIC TEST The vectographic test is an excellent test for suppression. The test consists of two superimposed polarized slides of letters that are projected onto an aluminized screen which reﬂects the images while preserving polarization. The patient is asked to read the letters on the screen while wearing polarized glasses. The polarization of the glasses and the projected slides are oriented so some of the letters are only seen by the right eye, some are only seen by the left eye, and some are seen by both eyes (Fig. 6-26). Patients with normal bifoveal fusion will see all the letters. If suppression is present, the letters projected only to the suppressed eye will not be seen (Fig. 6-27). Some patients with suppression will alternate ﬁxation and will see all the letters, although viewing them separately.

FOUR BASE-OUT TEST This test is performed by ﬁrst placing a 4 PD base-out prism over one eye. In normal subjects, the 4 base-out test induces fusional convergence. Remember, there are two movements to prism convergence: ﬁrst, a version movement of both eyes in the direction of the apex of the prism, and second, a fusional vergence movement of the eye without the prism in toward the nose. With the 4 base-out test, the examiner must look carefully for the second convergence movement, as it is the sign of fusion. Patients without motor fusion and large regional suppression show no movement of either eye when the prism is placed over the nondominant eye (Fig. 6-28A) and a version (not vergence) movement of both eyes in the direction of the apex of the prism when the prism is placed over the ﬁxing eye (Fig. 6-28B).

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FIGURE 6-26. Diagrammatic representation of vectograph with polarized glasses in place and lenses oriented 90° to each other. Letters are projected to a screen through two polarized lenses, which are also oriented 90° to each other and match the orientation of the glasses. In this patient with normal binocular vision, the left eye sees AC, right eye sees AB, and the perception is ABC, which is noted in the rectangle at the bottom of the ﬁgure.

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FIGURE 6-27. Diagram of vectograph examination of a patient with a suppression scotoma, left eye. In this case, the patient only sees images from the right eye and reports seeing an AB.

Patients with the monoﬁxation syndrome and a small central scotoma usually show no movement when the 4 PD prism is placed over the nondominant eye. Because these patients have peripheral fusion, monoﬁxators occasionally show a normal fusional convergence movement. A prism over the ﬁxing eye always results in a version movement in monoﬁxa-

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tors, and some will show fusional convergence movement as well. Normal patients with bifoveal fusion often show atypical responses to the 4 base-out test.5 Some normals fail to fuse the 4 PD base-out prism, showing an initial version movement but no secondary fusional convergence movement. These patients often alternate ﬁxation and report alternating diplopia. Other normals seem to ignore the induced phoria and show no move-

A

B FIGURE 6-28A,B. (A) Esotropia, left eye ﬁxing, right eye deviated with large suppression scotoma. Placing the 4 base-out prism in front of the deviated right eye produces no movement of either eye, because the image falls within the suppression scotoma. (B) Placing the 4 base-out prism in front of the ﬁxing eye results in a version movement, with both eyes moving in the direction of the apex of the prism, because there is no suppression scotoma and the movement of the image is perceived.

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ment when the 4 base-out prism is placed over one eye. Thus, a secondary fusional convergence movement on 4 base-out prism testing indicates fusion (central fusion or even peripheral fusion), but because of frequent atypical responses in normals, absence of a convergence movement does not necessarily mean an absence of fusion.

References 1. Ellis FD, Schlaegel TF. Unexpected visual recovery: organic amblyopia? Am Orthopt J 1991;31:7. 2. Kushner BJ. Abnormal sensory ﬁndings secondary to monocular cataracts in children and strabismic adults. Am J Ophthalmol 1986; 102(3):349–352. 3. Parks MM. The monoﬁxation syndrome. Trans Am Ophthalmol Soc 1969;1242–1246. 4. Pratt-Johnson JA, Tillson G. Intractable diplopia after vision restoration in unilateral cataract. Am J Ophthalmol 1989;107:23. 5. Romano PE, von Noorden GK. Atypical responses to the four-diopter prism test. Am J Ophthalmol 1969;67:935. 6. Sharkey JA, Sellar PW. Horror fusionis: a report of ﬁve patients. J Am Optom Assoc 1999;667(12):733–739. 7. Vereecken EP, Brabant P. Prognosis for vision in amblyopia after the loss of the good eye. Arch Ophthalmol 1984;102:220. 8. Wong AMF, Lueder GT, Burkhalter A, Tychsen L. Anomalous retinal correspondence: neuroanatomic mechanism in strabismic monkeys and clinical ﬁndings in strabismic children. JAAPOS 2000:168–174. 9. Wright KW, Fox BES, Erikson KJ. P-VEP evidence of true suppression in adult onset strabismus. J Pediatr Ophthalmol Strabismus 1990;27: 196–201. 10. Wright KW, Hwang JM. Diplopia and strabismus after retinal and glaucoma surgery. Am Orthopt J 1994;44:26–30.

7 Esodeviations Kenneth W. Wright

I

n contrast to exodeviations, which are usually acquired and intermittent, esodeviations often present as a constant esotropia occurring in infancy or early childhood. Fusional divergence is used to correct for an esodeviation; however, our innate divergence amplitudes are typically weak, measuring only 6 to 8 prism diopters (PD). It is likely that our weak divergence amplitudes contribute to the poor control of esodeviation. Because of the early onset and constant character of esodeviations, they tend to disrupt binocular visual development and are often associated with amblyopia, poor binocular fusion and minimal to no stereopsis. Exodeviations, on the other hand, are characteristically controlled by our strong convergence, highgrade stereoacuity, and amblyopia is rare. It is probable that our strong innate fusional convergence amplitudes of more than 30 PD allow exodeviations to be better controlled than esodeviations. Not all esotropic patients have a poor prognosis for binocular vision. Patients with late-onset acquired or intermittent esotropia usually have binocular fusion potential. The duration of the esotropia is an important factor that determines binocular fusion potential.40 Esodeviations can be classiﬁed into the categories outlined in Table 7-1.

CONGENITAL–INFANTILE ESOTROPIA Deﬁnition and Incidence Infantile esotropia, or, as it is often termed, congenital esotropia, is classically deﬁned as a large-angle esotropia that is present before 6 months of age (Fig. 7-1). Congenital esotropia is less common than the 1% reported in many texts. Mohoney et al.45 217

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TABLE 7-1. Types of Esotropia. Congenital-infantile esotropia (uncommon) Accommodative esotropia (common) Acquired nonaccommodative esotropia (uncommon) Esotropia nystagmus face turn (uncommon) Cyclic esotropia (rare) Esophoria (common) Divergence insufﬁciency (uncommon) Sensory esotropia (common)

reported a birth prevalence of 27 per 10,000 live births, and Archer et al.2 estimated the incidence of esotropia to be 0.5% in a study of 582 infants.

Normal Neonatal Alignment It is well known that newborns usually do not have straight eyes. A large population study64 documented that 30% of normal neonates have straight eyes, 70% have a transient exotropia or a variable angle strabismus, and less than 1% have esotropia. In that study, only 2 of 2271 neonates had an esotropia at birth and, in both cases, the esotropia resolved by 2 months of age.2 This

FIGURE 7-1. Four-month-old with the classic large-angle esotropia characteristic of infantile esotropia. The right eye is ﬁxing; the left eye is deviated.

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important study indicates that esotropia infrequently occurs at birth, whereas exodeviations are common.

Etiology Esotropia occurring in infancy can be caused by a variety of disorders including congenital ﬁbrosis of the extraocular muscles, Duane’s syndrome, and infantile myasthenia gravis (Table 7-2). In most of the ophthalmology literature, these rare secondary causes of esotropia are not included under the category of infantile esotropia. The etiology of primary infantile esotropia is a source of controversy and remains unknown. Costenbader suggested that hypermetropia with overconvergence plays an important role.19 Historically, there have been two basic theories for the cause of congenital esotropia and the poor binocular sensory outcomes after treatment: the Worth theory and Chavasse theory. The Worth theory states that the esotropia is caused by a congenital absence of cortical fusion potential. This theory places the blame on a primary cortical fusion deﬁcit present at birth and states there is no hope for obtaining good binocular function. The Chavasse theory contends that congenital esotropia represents a primary motor misalignment, and the poor binocular sensory status so often seen in these patients is secondary to a disruption of binocular visual development caused by the infantile strabismus. Chavasse supporters speculate that patients with congenital esotropia have binocular cortical potential for high-grade stereopsis and fusion but that the presence of an esotropia during the early period of binocular visual development permanently damages binocular function.

TABLE 7-2. Differential Diagnosis of Infantile Esotropia. Pseudo-esotropia Congenital esotropia Infantile accommodative esotropia Duane’s syndrome Sensory esotropia Congenital sixth nerve palsy, usually transient Möbius syndrome Congenital ﬁbrosis syndrome Infantile myasthenia gravis Neurological disease

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It is likely that infantile esotropia represents a heterogeneous syndrome composed of a variety of different sensory and motor abnormalities. Factors such as early weakness of the lateral rectus muscle, hypermetropia causing accommodative convergence, abnormalities of muscle anatomy, and lack or immaturity of cortical fusion may independently or collectively predispose to the development of esotropia. One possible cause for esotropia may relate to immaturity of sixth nerve function. The sixth and fourth cranial nerves are the longest nerves that innervate the extraocular muscles and are the last to fully myelinate. Perhaps there is a relative delay in sixth nerve maturation compared to the third nerve, which myelinates ﬁrst. A relative sixth nerve palsy occurring at birth or in the neonatal period might cause the medial rectus muscle to be unopposed, resulting in infantile esotropia. It is interesting to note that inferior oblique overaction frequently occurs in patients with infantile esotropia. Inferior oblique overaction may represent an early superior oblique paresis resulting from the long fourth nerve and delay in functional maturation. Whatever the cause or causes of infantile esotropia, there are compelling basic science and clinical studies indicating that esotropia occurring during the developmental period can permanently damage binocular vision. In addition, many infants with esotropia have the cortical potential for binocular fusion.7,21,33,37,71 These two important principles provide the basis for our treatment strategy.

Differential Diagnosis of Infantile Esotropia The differential diagnosis of infantile esotropia includes Duane’s syndrome, congenital ﬁbrosis syndrome, congenital sixth nerve palsy (Möbius syndrome associated with sixth nerve paresis), and infantile myasthenia gravis. These disorders all have limited abduction and, therefore, can be differentiated from infantile esotropia where the ductions should be full. This differentiation may be difﬁcult in patients with large-angle infantile esotropia and tight medial rectus muscles. Even in these patients, however, vestibular stimulation by doll’s head maneuver reveals full ductions and good abduction saccades. Other diagnoses include pseudo-esotropia secondary to large epicanthal folds and infantile accommodative esotropia. Infantile accommodative esotropia may be difﬁcult to distinguish from infantile esotropia. The key to the diagnosis of infantile

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accommodative esotropia is the presence of straight eyes for several months, followed by a variable small-angle esodeviation associated with hypermetropia of 3.00 or more. (See Infantile Accommodative Esotropia later in this chapter.)

Clinical Features Infantile esotropia is characterized by a large-angle esotropia presenting from birth to 6 months of age (see Fig. 7-1). There may be a history of the angle of deviation increasing during the ﬁrst few months of life.37 There is often some limitation of abduction to voluntary version testing; however, doll’s head maneuver and abduction saccades reveal normal lateral rectus function. The majority of children will be in good health otherwise, but there are some systemic associations that are well known.

Onset The age of onset of infantile esotropia and whether it is truly congenital or acquired has been controversial. Nixon et al. reported no cases of constant esotropia among 1219 newborns, indirectly suggesting that onset in many cases is postnatal.49 In contrast, the Congenital Esotropia Observational Study (CEOS) multicenter study sponsored by the NIH (this author was study chairman) found that 43% of large-angle infantile esotropia cases were reported by the parent or guardian to have occurred at birth, whereas 23% were ﬁrst noted after the ﬁrst month of life.51 In a study of 3324 newborns, Archer et al.2 found three cases documented to have straight eyes at birth, later acquiring esotropia at 2 to 4 months of age. In summary, it seems that the onset of the esotropia is variable, with some cases being truly congenital while others are acquired, even several months after birth.

Character of the Esotropia Infantile esotropia has been classically described as a large-angle constant esotropia. For the most part, this has been based on retrospective case series of patients who had undergone strabismus surgery.28,31,48 The CEOS51 also showed that esotropia occurring in the ﬁrst few months of life is often small to moderate in size and is frequently variable or intermittent. In this

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multicenter study of 2- to 3-month-old infants with esotropia, 56% of patients were characterized as having a constant esotropia, 25% a variable deviation, and 19% had an intermittent esotropia. Only half had a deviation measured to be 40 PD or greater. Larger deviations tended to be constant, whereas the majority of the smaller-angle deviations were intermittent or variable.

Spontaneous Resolution of Esotropia Until the data from the CEOS collaborative group52 became available, there was limited information on spontaneous resolution of early-onset esotropia. Birch et al.5 prospectively followed 80 infants with esotropia who were ﬁrst seen at 2 to 4 months of age. Resolution without surgery occurred at 6 months of age in 3 of 8 patients whose initial deviation was intermittent or variable, 3 of 23 patients with a constant esotropia of 35 PD or less (2 of whom were given spectacle correction for hypermetropia), and 0 of 49 with a constant esotropia of 40 PD or more. Clarke and Noel16 described 3 cases of constant esotropia diagnosed by 6 months of age that spontaneously decreased to less than 10 PD after 1 year of age but retained persistent signs of abnormal motor development including dissociated vertical deviation and latent nystagmus. Friedrich and de Decker27 described 1 case of a transient variable large-angle esotropia and 6 cases of small- to moderate-angle, mostly intermittent, esotropia ﬁrst noted between 1 and 3 months, of age, that spontaneously resolved. The ﬁndings of CEOS provide the best data on spontaneous resolution of infantile esotropia.52 This multicenter prospective study found of 170 patients, 46 (27%) spontaneously resolved to within 8 PD of orthotropia at the outcome exam either with or without spectacle correction. Patients with a small angle () 40 PD, and intermittent esotropia had a 50% to 78% rate of spontaneous resolution. In contrast only 2 of (3%) 64 patients with a constant esotropia of 40 PD or more on both the baseline and ﬁrst follow-up exam and with a refractive error of 3.00 diopters or less, the esotropia resolved at the outcome exam. One patient had a persistent 40 PD esotropia at the outcome exam; however, the esotropia improved without treatment to ET 5 PD. The conclusion of CEOS was that early-onset esotropia frequently resolves if the esotropia is less than 40 PD and is intermittent or variable. If the esotropia is constant or greater than 40 PD pre-

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senting on 2 exams with less than 3.00 D refractive error, then the likelihood of spontaneous resolution is remote. Ing37 reported that in 41 cases of esotropia seen at an average age of 6 months, the esotropia increased between the ﬁrst examination and the time of surgery by 10 PD or more in 61% and did not decrease by 10 PD or more in any patients. Because this was a retrospective study of patients who had undergone strabismus surgery, there might have been a selection bias for patients with an increasing esotropia. Thus, spontaneous resolution of infantile esotropia does occur, especially if the deviation is small, variable, or intermittent. However, infants with a constant deviation of 40 PD or more on two exams and with less than 3.00 D of hyperopia have a low likelihood of spontaneous resolution and can be considered for early surgery.

Amblyopia Associated with Infantile Esotropia The ability to alternate ﬁxation, or hold ﬁxation well with either eye, indicates equal vision (Fig. 7-2).72 Strong ﬁxation preference, on the other hand, indicates amblyopia of the nonpreferred eye, and should be treated by patching the preferred eye before strabismus surgery.72 The incidence of amblyopia seems to be proportional to the duration of the esotropia. In the CEOS,51 amblyopia was diagnosed in 19% of patients at the ﬁrst visit (2 months of age) and doubled to 42% at subsequent visits (after 6 months of age). This frequency is similar to the 22% rate reported by Hiles et al.31 and to the 13% rate reported by Hoyt et al.32 for patients examined before 1 year of age. Higher rates of amblyopia (41%–72%) have been reported in postsurgical case series extending over many years of follow-up.19,59 Some have blamed surgery for causing amblyopia because the rates of amblyopia were higher in the postsurgery patients. It is more likely, however, that this higher rate of amblyopia reﬂects the higher incidence of amblyopia having a longer duration of esotropia.

Refractive Error Costenbader found that more than half of 500 children with congenital esotropia had signiﬁcant hypermetropia ranging from 2.25 to over 5.00.19 The CEOS showed that mild to moderate hypermetropia was present in most patients, with about 20%

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A

B FIGURE 7-2A,B. Patient with infantile esotropia and alternating ﬁxation, no amblyopia. (A) Patient is ﬁxing with the right eye. (B) Patient is ﬁxing with the left eye.

being above 3.00 D, 12% above 4.00 D, and less than 10% being myopic.51 Similar results have been reported in other infantile esotropia series, as Birch et al.8 found 17% of cases and Ing39 found 25% of cases with hyperopia of 3.00 or more. In a

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31

series by Hiles et al. on older children, hyperopia greater than 3.00 D was present in 15% of the 54 cases. Mutti et al.47 reported similar incidence of refractive errors in a study of 288 normal 3-month-old infants with a mean refractive error of 2.10 1.3 D; 21% were greater than 3.00 D, 8% were greater than 4.00 D, and 3% had myopia of 0.50 D or greater. It seems, from a review of the literature, that infants with esotropia have, on average, refractive errors similar to the normal age-matched population. There are selected patients, however, with moderate to high hypermetropia who appear to have esotropia on the basis of accommodative convergence.

Associated Motor Abnormalities The classic triad of motor abnormalities associated with congenital esotropia is inferior oblique overaction, dissociated vertical deviation (DVD), and latent nystagmus.36 These three associated ﬁndings may occur individually or in any combination and usually become manifest some time after 1 year of age.68 CEOS found inferior oblique overaction and DVD to be almost nonexistent at the initial exam at approximately 2 months of age.51 Eight percent (8%) of patients had inferior oblique overaction and 4% had DVD at 6 months of age.51 Hiles et al.31 reported the rate of 15% for inferior oblique overaction and 2% for DVD between 3 and 10 months of age, but both increased to approximately 75% at long-term follow-up examinations. (See Chapter 9 for a discussion of inferior oblique overaction and Chapter 10 for DVD.) Latent nystagmus occurs less frequently than inferior oblique overaction or DVD. CEOS51 found only a 4% frequency at 6 months of age, and Robb and Rodier59 reported a frequency of 16%. Smooth pursuit asymmetry is another motor ﬁnding present in virtually all patients with infantile esotropia (see Chapter 4, p. 158).1,65 Smooth pursuit asymmetry is a marker of early disruption of binocular visual development.

LATENT NYSTAGMUS Latent nystagmus is a bilateral nystagmus that becomes manifest when one eye is occluded, or the eyes are dissociated by blurring the vision of one eye, or by suppression of one eye associated with manifest strabismus; this is a jerk-type nystagmus with the fast phase toward the ﬁxing eye. Velocity recordings show that

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the velocity of the slow phase decreases toward the end of the slow-phase eye movement (decreasing velocity slow phase).23 Latent nystagmus is also associated with conditions that disrupt early binocular visual development, such as congenital monocular cataracts.

Systemic Associations In most cases, congenital esotropia occurs as an isolated problem in an otherwise healthy child; however, it can be associated with systemic diseases such as Down’s syndrome, albinism, and cerebral palsy. The differential diagnosis of esotropia occurring in infancy includes Möbius syndrome, congenital ﬁbrosis syndrome, Duane’s syndrome, infantile myasthenia gravis, and congenital sixth nerve palsy. Congenital sixth nerve palsy is rare and usually spontaneously resolves over a few weeks. Neurological processes such as hydrocephalus and intracranial tumors can present as an infantile esotropia. Most clinical studies on congenital esotropia exclude patients with neurological or systemic disease. Thus, congenital esotropia is usually deﬁned as a primary esotropia not associated with a sixth nerve palsy, a neurological condition, or a signiﬁcant restriction, and occurs before 6 months of age.

Clinical Assessment Evaluation should start with amblyopia assessment, usually by ﬁxation preference. Assessment of ductions and versions are important to diagnoses an abduction deﬁcit possibly related to a sixth nerve palsy or oblique dysfunction. Patients with infantile esotropia often show some limitation of abduction. In these cases, it is important to verify the abduction deﬁcit by vestibular stimulation with the doll’s head maneuver or by spinning the infant. Vestibular stimulation is best performed in infants by gently spinning the child (Fig. 7-3). Many children who show an abduction deﬁcit to voluntary abduction will have full abductions by vestibular stimulation. If an abduction deﬁcit persists, assess lateral rectus function by examining the abduction saccade. If there is a brisk abduction saccade, then the lateral rectus is functioning and the limited abduction is restrictive, probably secondary to a tight medial rectus muscle. A slow or absent abduction saccade indicates a weak lateral rectus, possibly caused by a sixth nerve palsy or a Duane’s syndrome. Opto-

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FIGURE 7-3. Diagram of an infant in examiner’s hands. Infant is moved to the right, which stimulates eye movement to the left. If the right eye fully abducts, then lateral rectus function is normal and there is no signiﬁcant restriction of the medial rectus muscle. Spinning an infant will cause the eyes to move opposite to the spin, an excellent way to examine horizontal ductions in an otherwise uncooperative infant.

kinetic stimulation (OKN drum or tape) is a good way to stimulate saccadic eye movements.69 The angle of deviation is measured by cover/uncover testing or with Krimsky light reﬂex, and near and distance measurements should be obtained if possible. A cycloplegic refraction and a dilated fundus exam are also indicated.

Inheritance The inheritance of congenital esotropia remains undeﬁned; however, it is well known that it runs in families.44,45,55 Affected family members may have congenital esotropia, but other types of strabismus are often found, including accommodative esotropia and congenital superior oblique palsy. Maumenee et al.,44 in an analysis of a large group of families, concluded that the inheritance is consistent with a Mendelian codominant model in which there is an admixture of primarily autosomal recessive cases, some dominant cases, and possibly nongenetic

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cases. Variable patterns of inheritance for infantile esotropia speak to the heterogeneity of this syndrome. In CEOS,52 a family history of strabismus was reported for 45% of patients, with 29% having a family history in a ﬁrst-degree relative, according to parental report. Similarly, a study by Mohoney et al.45 found a family history of strabismus in 34% of cases of early-onset esotropia compared with this history in 12% of matched controls, and Shauly et al.61 reported 44% of patients who had a history of strabismus. These studies, however, do not distinguish between early-onset esotropia and other forms of strabismus.

Types of Infantile Esotropia PSEUDO-ESOTROPIA Pseudo-esotropia is a condition in which the eyes are orthotropic but appear to be crossed; this usually occurs in infants who have a wide nasal bridge with prominent epicanthal folds (Fig. 7-4). Pseudo-esotropia usually resolves by 2 or 3 years of age because the epicanthal folds diminish as the bridge of the nose enlarges. Patients with a small interpupillary distance may also appear to be esotropic, especially when the eyes are in sidegaze or are focusing at near. Often, parents bring photographs that show the child’s eye “turned in.” Close examination of these photographs often reveals that the photograph was taken with the child’s head turned and the eyes in sidegaze. The eye that is turned nasally is buried under the epicanthal fold. Children with pseudo-strabismus should have a full ocular examination. It is important to follow these children, as a small percentage will end up having a true esodeviation.

INFANTILE ACCOMMODATIVE ESOTROPIA Accommodative esotropia can occur in babies as young as 2 months of age and are often classiﬁed under the diagnosis of “congenital esotropia.” These infants should be immediately treated with their full hypermetropic correction (see Infantile Accommodative Esotropia later in this chapter).

CIANCIA’S SYNDROME Ciancia’s syndrome is a large-angle congenital esotropia with cross-ﬁxation, and both eyes appear to be “stuck” in toward the nose. It consists of the following characteristics: (1) large-angle

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A

B FIGURE 7-4A,B. Pseudo-strabismus. (A) Note the large epicanthal folds giving the appearance of esotropia even though the eyes are well aligned. (B) Pinching the epicanthal skin folds demonstrates the eyes are well aligned.

deviation (60 PD), (2) bilateral limited abduction with intact abduction saccades, (3) ﬁxing eye in adduction, (4) nystagmus on attempted abduction with no nystagmus in adduction, and (5) face turn to the side of the ﬁxing eye (Fig. 7-5). In Ciancia’s

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A

B FIGURE 7-5A,B. Patient has Ciancia’s syndrome with bilateral tight medial rectus muscles causing a large-angle esotropia and limited abduction. The patient is most comfortable with the ﬁxing eye in adduction. To establish this, the patient adopts a face turn toward the ﬁxing eye, thus placing the ﬁxing eye in adduction. In (A), the patient is ﬁxing the right eye, with face turn to the right; in (B), patient is ﬁxing the left eye and has a face turn to the left. This patient with Ciancia’s syndrome is showing a pattern of cross-ﬁxation.

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syndrome, the abduction deﬁcit is most likely secondary to tight medial rectus muscles. Clinical examination shows good lateral rectus function, evidenced by normal brisk abduction saccades. Forced duction at the time of surgery shows moderately tight medial rectus muscles. The abduction nystagmus is a subtle jerk nystagmus with the fast phase in the direction of the ﬁxing eye and only occurs when the ﬁxing eye abducts. This nystagmus probably represents an exaggerated endpoint nystagmus, as the lateral rectus muscle pulls against the tight medial rectus muscles. Ciancia found that approximately one-third of his patients with congenital esotropia had this syndrome.15 It is likely that many of the patients described by Ciancia would have been classiﬁed in the American literature as large-angle congenital esotropia with cross-ﬁxation. The reason for the face turn in these patients with a large-angle esotropia, and the ﬁxing eye in adduction is probably not to damp the nystagmus, as the nystagmus is usually minimal if present at all; the face turn is adopted because the medial rectus is tight and holds the ﬁxing eye in adduction. Surgically correcting the esotropia associated with Ciancia’s syndrome is difﬁcult, as undercorrections are frequent. One of the problems is measuring the full deviation, as both eyes are “stuck” in adduction and it is difﬁcult to get the ﬁxing eye into primary position for a true measurement. The surgery of choice is large medial rectus recessions, approximately 7 mm posterior to the insertion site.57

CROSS-FIXATION Patients with limited abduction and tight medial rectus muscles adopt a face turn to ﬁxate with an eye in adduction; probably the same syndrome described by Ciancia (see Ciancia Syndrome above). These patients may cross-ﬁxate, ﬁxing with the right eye for objects in the left visual ﬁeld and ﬁxing with the left eye for objects in the right visual ﬁeld. Cross-ﬁxation was once seen as a sign of equal vision, but Dickey et al.24 reported that crossﬁxators can have mild amblyopia. Patients have true equal vision if they can hold ﬁxation with either eye through smooth pursuit, without reﬁxating to the fellow eye.

CONGENITAL FIBROSIS SYNDROME This syndrome is a congenital restrictive strabismus, often inherited as an autosomal dominant trait (see Chapter 10). Con-

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genital ﬁbrosis syndrome may cause virtually any horizontal or vertical strabismus and is associated with extremely tight ﬁbrotic rectus muscles on forced duction testing. It frequently presents as a large-angle congenital esotropia with severe limitation of abduction of one or both eyes; this has also been termed strabismus ﬁxus. Even though abduction is severely restricted, OKN stimulus or the doll’s head maneuver will show abduction saccadic eye movements of brisk, albeit small, amplitudes, indicating intact lateral rectus function.

Treatment of Congenital Esotropia The treatment of congenital esotropia (ET) is usually surgical. Occasionally, infants with esotropia may be corrected with hypermetropic spectacle correction. Spectacles should be tried in small-angle cases (ET 40) if hypermetropia is 2.00 or greater and in patients with large-angle esotropia ( 40 PD) if the hypermetropic correction is 3.00 or more. Birch et al.8 reported that 3 of 84 infants with esotropia of at least 30 PD seen at 2 to 4 months of age achieved alignment with spectacle correction and required no surgery. It is important to fully treat amblyopia before performing surgery, with the endpoint of patching being “holds ﬁxation well” with either eye by ﬁxation preference testing. If the child is cosmetically straightened by the surgery, the parents may consider that the problem is cured and they may not return for amblyopia treatment. The only situation when surgery is indicated in the face of residual amblyopia is a tight medial rectus muscle that causes one eye to be buried in the medial canthus even when the good eye is patched as this blocks the vision of the amblyopic eye and makes effective amblyopia therapy impossible. This unusual problem most frequently occurs in association with strabismus ﬁxus of congenital ﬁbrosis syndrome or, rarely, Ciancia’s syndrome. The standard surgical approach is bilateral medial rectus recessions using the standard surgical charts (see endpapers). The amount of recession is usually based on the near deviation as it is difﬁcult to obtain accurate distance measurements in infants. In young infants with fusion potential, a small postoperative exodeviation is probably desirable to allow fusional convergence to align the eyes.60 In older patients with irreversible signiﬁcant amblyopia, limit surgery to the amblyopic

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eye by performing a recession of the medial rectus muscle and a resection of the lateral rectus muscle.

PROGNOSIS AND TIMING OF SURGERY There are few long-term outcome studies on congenital esotropia and these are retrospective.30,31,61 Historically, alignment and sensory outcomes for patients have been poor using the standard approach of operating late between 6 months to 2 years of age. Except for rare cases, the best results with standard surgery have been monoﬁxation with peripheral fusion and only gross stereopsis. Monoﬁxation and peripheral fusion, however, do not guarantee long-term stability, as many patients will lose binocular fusion over time.3,63 There is growing evidence that outcomes from surgery for infantile esotropia can be improved by early intervention to align the eyes as soon the diagnosis is ﬁrmly established, even operating before 6 months of age. The best time to operate on infantile esotropia remains controversial.11,17,30,62,71 At the time of this printing, this author suggests operating for infantile esotropia as early as 12 to 13 weeks of age, so long as the esotropia is a constant tropia greater than 40 PD and there have been two examinations (3–4 weeks apart) documenting that the deviation is stable or increasing. Infants with small to moderate deviations, intermittent deviations, or variable-angle esotropia are observed until 6 months of age or longer. CEOS data show that these patients have a signiﬁcant rate of spontaneous resolution. In infants under 5 months of age, this author performs bilateral medial rectus recessions using the standard tables, with a maximum recession of 6.0 to 6.5 mm posterior to the medial rectus muscle insertion.

RATIONALE FOR EARLY SURGERY The rationale for performing early surgery for infantile esotropia is derived from basic science research and clinical studies. Hubel and Wiesel were among the ﬁrst to show that strabismus occurring during the early period of visual development causes permanent loss of binocular cortical cells and disruption of binocular visual development.33 Studies by Crawford and von Noorden21,22 and Crawford et al.20 have shown that as little as 3 weeks of prism-induced esotropia will cause permanent loss of binocular cells and stereopsis in infant monkeys. Importantly,

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A

B FIGURE 7-6A,B. Chart from the study by Crawford and von Noorden21,22 shows the results of prism-induced esotropia in infant monkeys. Column A shows the normal distribution of occipital cortex with the largest spike in the center representing binocular cells (B) and fewer monocular cells (R, right eye; L, left eye). Columns B through E represent the cortical cell distribution after increasing duration of prism-induced esotropia. Note that after only 20 days of prism-induced esotropia (column C), almost all the binocular cortical cells are gone and there is a corresponding increase in monocular cells. Column F plots the binocular cell loss over time from prism-induced esotropia and shows an inverse relationship, with longer duration of esotropia corresponding to fewer binocular cells.

loss of binocular cells after brief periods of prism-induced esotropia persisted after removing the prisms, even after allowing up to 3 years for recovery. These studies also demonstrated that the loss of binocularity is directly proportional to the duration of the esotropia (Fig. 7-6).

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In humans, the critical period for the development of binocular vision appears to be the ﬁrst 3 to 4 months of life.6,12,25,41,71 Stereopsis develops rapidly and is nearly completed in infancy.6,41,53 Birch and Stager10 have demonstrated that, by 5 months of age, about 40% of esotropes corrected with prisms had stereopsis, similar to that found in infants of this age with normal visual development. After 5 months of age, only about 20% of the early-onset esotropes demonstrated stereopsis, in contrast to 100% of normal infants. The timetable for the development of binocular fusion may be even earlier, as this author has personally seen compensatory head posturing and a gaze preference associated with incomitant strabismus in infants as young as 3 weeks, thus indicating the presence of binocular fusion. It is likely that stereoacuity improved with increasing visual experience as visual acuity improved. Clinical studies clearly indicate that early surgery before 1 to 2 years of age is critical to obtaining some binocular fusion, at least peripheral fusion. Ing,35 in a landmark article, demonstrated the importance of early surgery, reporting that approximately 80% of congenital esotropic patients achieved peripheral fusion if aligned before 2 years of age. In contrast, patients aligned after 2 years of age had less than 20% chance of obtaining any fusion. In addition to being a consummate clinician scientist, Dr. Ing is a champion surfer (Fig. 7-7). More recent studies indicate that surgery performed before 1 year of age results in even better binocular function and estab-

FIGURE 7-7. Photograph of Dr. Malcolm Ing surﬁng at his home in Hawaii with Diamond Head in the background. Dr. Ing’s landmark work on early surgery for congenital esotropia has made a tremendous improvement in the care of our patients.

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lishes random dot stereoacuity.40,50,99 Very early surgery, that is, before 6 months of age, remains controversial, but it appears to be safe and may provide the best sensory outcomes.30,71 Helveston et al.30 reported results on 10 infants operated for infantile esotropia between 12 and 23 weeks of age. All achieved a ﬁnal alignment within 10 PD of orthotropia, although many required reoperation, as the follow-up was as long as 10 years. Four patients obtained stereoacuity, 1 with 140 s arc. In 1994, this author reported results of very early surgery on 7 infants operated between 13 and 19 weeks of age with a follow-up of 2 to 8 years (mean, 4.1 years). All had excellent alignment at the ﬁnal visit with a tropia of 8 PD or less. Five of the 7 required only one operation to obtain good alignment, and 2 required one reoperation. Five children could cooperate with stereo testing at the outcome examination and all 5 showed stereoacuity ranging from 400 to 40 s arc. Three children achieved high-grade stereoacuity by random dot testing and 2 had 40 s arc. Figures 7-8 and 7-9 show pre- and postoperative photographs of the two patients who obtained 40 s arc stereoacuity after very early surgery. The basic science data and clinical studies suggest that many patients with infantile esotropia do have the potential for

A FIGURE 7-8A. Early surgery for congenital esotropia patient. (A) Photograph of 1-week-old infant with congenital esotropia. Patient’s grandfather is a physician and noted esotropia at birth.

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B

C FIGURE 7-8B–C. (B) Surgery was performed at 13 weeks of age. Photograph taken 1 day after bilateral medial rectus recessions, 6.0 mm, showing consecutive exotropia. The exotropia was intermittent and resolved a few days after surgery. (C) Same patient at 5 years of age. Early surgery resulted in excellent alignment with best binocular sensory result ever reported. The patient has now been followed for more than 7 years with straight eyes, no dissociated vertical deviation, no latent nystagmus, and no inferior oblique overaction; fusion of Worth 4-dot in the distance and near, 40 s of stereo by Titmus testing, and Randot stereopsis. The only binocular functional defect is trace optokinetic nystagmus (OKN) asymmetry seen only by electro-oculogram (EOG) recording; no OKN asymmetry is seen clinically.

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A

B FIGURE 7-9A–B. Early surgery for congenital esotropia patient. (A) Preoperative photograph of patient with infantile esotropia at 19 weeks of age. (B) Postoperative day 1 with a consecutive exotropia; this was intermittent and lasted only a day or two.

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C

D FIGURE 7-9C–D. (C) Photograph taken at age 8 years. Patient had 40 s stereoacuity, with slight intermittent exotropia. One year later, patient underwent bilateral lateral rectus recessions for an exotropia. (D) At a recent follow-up visit at 14 years of age, patient maintains excellent alignment and 40 s stereoacuity after early surgery for infantile esotropia.

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stereopsis if surgically aligned early, prior to 1 year of age. In addition, very early surgery, before 6 months and even as young as 3 months of age, appears to be safe and may be of critical importance for establishing a high level of binocular fusion and stereopsis. It is likely that an important factor is to reduce the duration of the esotropia.

GOOD STEREOPSIS WITH LATE SURGERY As already described, basic science research in nonhuman primates has demonstrated that brief periods of strabismus (as little as 3–4 weeks) during the neonatal period will permanently disrupt binocular function. Despite these studies, there have been sporadic cases of infantile esotropia that demonstrated stereoacuity following “late” surgery, even in adulthood (Fig. 7-10).45 In fact, two patients in Ing’s 1981 study35 achieved 40 s arc stereoacuity even though the eyes were surgically aligned after 1 year of age. It is likely that some infants who are classiﬁed as having early-onset esotropia actually have straight eyes or intermittent esotropia during the ﬁrst few months of life, probably establishing binocular cortical cells needed for fusion. Perhaps, once established in early infancy, binocularity may be reestablished later in life when the eyes are aligned after strabismus surgery. Because some patients with presumed congenital-onset esotropia achieve binocular fusion after late surgery, we should not categorically assume an older patient with esotropia does not have fusion potential.

POSTOPERATIVE CARE All patients with congenital esotropia should be followed closely for amblyopia, even if good motor alignment is achieved. The goal of surgery is to obtain alignment within 8 to 10 PD of orthotropia to allow for the establishment of peripheral fusion and the monoﬁxation syndrome. Deviations larger than 10 PD preclude the development of even peripheral fusion. Postoperative tropias greater than 10 PD should be treated with either further surgery or spectacle correction.

Consecutive Exotropia An initial small-angle exotropia is probably desirable in infants young enough to have fusion potential; however, a persistent exotropia 4 to 6 weeks after surgery may require additional

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A

B FIGURE 7-10A,B. (A) Preoperative photograph of teenager with a largeangle esotropia that mother thinks was present since birth. Patient had no previous surgery. (B) Postoperatively after bilateral medial rectus recessions, the patient achieved excellent alignment, and peripheral fusion with gross stereoacuity. Old records revealed the patient to be hypermetropic, and the patient probably had an intermittent esotropia acquired during late infancy. If fusion is established in infancy, it is often retrievable later, in contrast to a constant congenital esotropia, which has a poor prognosis for fusion if alignment is delayed.

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surgery. If the consecutive exotropia increases in sidegaze or is associated with an adduction deﬁcit, consider the possibility of a slipped muscle or stretched scar. Explore the medial rectus muscles if there is a question of muscle stability, as a stretched scar or slipped medial rectus muscle is fairly common. For the advancement procedure, this author now prefers a nonabsorbable suture or a long-lasting absorbable suture. The treatment of choice for a consecutive exotropia without a slipped muscle is bilateral lateral rectus recessions.

Residual Esotropia A residual esotropia greater than 10 to 15 PD that persists longer than 6 to 8 weeks after surgery should be treated. The ﬁrst line of treatment is to give the full hypermetropic spectacle correction if the cycloplegic refraction is 1.50 or more. If there continues to be a signiﬁcant esotropia after glasses are prescribed or there is not enough hypermetropia to warrant glasses, then surgery should be considered, especially if the child is under 2 years of age and there is fusion potential. If the initial recession was 5.0 mm or less, this author prefers a rerecession of one or both of the medial rectus muscles. A bilateral 2-mm re-recession corrects roughly 20 to 25 PD of residual esotropia. Patients with residual esotropia and initial recessions greater than 5.0 mm should be managed with lateral rectus resections, doing slightly less than described on the standard charts. Because a previously recessed medial rectus muscle is being resected, remember to do a slightly smaller resection to avoid an overcorrection. An alternative to surgery in cases of small residual esotropia is prescribing base-out prism glasses.

The Role of Botulinum Toxin In addition to surgery, some have advocated the use of botulinum for the treatment of congenital esotropia. The theoretical advantage would be to create an incomitant deviation so the patient could adopt a face turn and obtain fusion. Although this has theoretical merit, there are some problems involved with the use of botulinum. These complications include secondary ptosis, initial consecutive exotropia lasting up to 2 to 3 months, and the temporary effect of the botulin injection itself. Most studies have shown that multiple injections are needed to sustain the effect.43 Even with multiple injections, alignment

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and sensory outcomes have been signiﬁcantly worse than surgery.38 The treatment of choice for most patients with congenital esotropia remains surgical.

ACCOMMODATIVE ESOTROPIA Accommodative esotropia is usually associated with signiﬁcant hypermetropia of 2.00 or more and is termed hypermetropic accommodative esotropia, or refractive esotropia. Prescribing the full hypermetropic spectacle correction will improve or, in many cases, totally correct the esotropia. Some patients with accommodative esotropia have a high AC/A ratio esotropia, meaning that they have a greater deviation at near versus distance. They are usually hypermetropic, but may be emmetropic or even myopic. Acquired esotropia deserves an urgent consultation. Delay of treatment will reduce the chances for reestablishing binocular fusion.25 In addition, acquired esotropia may represent a neurological process, so urgent evaluation is important.

HYPERMETROPIC ACCOMMODATIVE ESOTROPIA Etiology Hypermetropic accommodative esotropia is caused by accommodative convergence associated with hypermetropia. These children have straight eyes as infants but, as they learn to accommodate to correct for their hypermetropia, they overconverge and develop esotropia. A child with hypermetropia of 3.00 would have to accommodate 3 diopters to create a clear retinal image for distance viewing. If the AC/A ratio is 6 (high normal), the accommodative convergence will produce an esodeviation of 18 PD. Depending on the patient’s divergence fusional amplitudes, this patient may develop an esodeviation.

Clinical Features Accommodative esotropia usually presents as an acquired intermittent esotropia. The onset ranges from infancy to late childhood, most commonly occurring around 2 years of age. The size

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of a deviation is variable and is typically smaller than congenital esotropia, usually measuring between 20 and 40 PD. Cycloplegic refraction reveals hypermetropia between 1.50 and 6.50 diopters. Parents often give a history that the eyes are straight some of the time; however, when the child is tired or focusing at near, the eyes will cross. The esotropia is initially intermittent but may quickly increase to become a constant deviation. Patients with constant esotropia may lose fusion potential and are prone to develop amblyopia.

Cycloplegic Refraction An accurate cycloplegic refraction is required to determine the full hypermetropic correction. Young children are often difﬁcult to refract, and repeat cycloplegic refractions help ensure accuracy. Cyclopentolate is the standard cycloplegic agent. Cyclopentolate is given topically, one or two doses for a lightly pigmented iris, and two or three doses for a dark iris. Consider using atropine in patients with a darkly pigmented iris who show variable retinoscopy readings. The refraction is performed 30 min after the last dose. Atropine is given twice a day for 3 days, and the refraction is done on the third day. The mydriatic effect of these drugs lasts much longer than the cycloplegic effect, so a dilated pupil does not mean complete cycloplegia.

Treatment The ﬁrst step in the treatment of hypermetropic accommodative esotropia is to prescribe the full hypermetropic correction (see example, following). In both juvenile-onset and infantileonset accommodative esotropia, full hypermetropic correction should be prescribed as soon as the esotropia is identiﬁed, even giving glasses to children as young as 2 months of age (Fig. 7-11). Delay in treatment can result in loss of binocular potential.25 Example 1. 2-year-old with esotropia for 2 months Full ductions and versions Cycloplegic refraction 4.50 OU Without correction (sc): With correction (cc) 4.00 OU: Dsc ET 30 Dcc E 4 (phoria) Nsc ET 35 Ncc E 2 (phoria) Treatment: Prescribe spectacles 4.50 sphere OU

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A

B FIGURE 7-11A,B. (A) Three-month-old infant with a 35 PD esotropia and 3.00 D refractive error. (B) Infant now with straight eyes wearing full hypermetropic correction.

It is important that the child wears the optical correction fulltime. Children who intermittently remove their glasses will not relax their accommodation and will have blurred vision with their appropriate hypermetropic correction. For children who have difﬁculty relaxing accommodation and therefore do not

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accept their hypermetropic correction, it may be helpful to prescribe a short course of cycloplegics such as atropine or cyclopentolate. Parents should be told that the glasses are prescribed to straighten the eyes by relaxing the overfocusing caused by the farsightedness. If, after prescribing full hypermetropic correction, the eyes are straightened to within 10 PD distance and near and the patient obtains binocular fusion, nothing more need be done but continue with the full hypermetropic correction. Some advocate reducing the plus lens until an esophoria is induced; to try to build fusional divergence and wean the child from glasses. This author has not seen this practice reduce the need for spectacles but, all too frequently, has seen it turn a well-controlled deviation into a manifest esotropia. By reducing the plus, you run the risk of producing a manifest esotropia and losing binocular fusion. Remember, children with accommodative esotropia have tenuous fusion. To establish binocular function, the goal must be to align the eyes to orthotropia. If, after wearing full hypermetropic spectacles for 4 to 8 weeks, a residual esotropia of more than 10 PD is present for distance and near (the patient is not fusing), then surgery is indicated. This residual deviation is termed partially accommodative esotropia (discussed later in this chapter). In some cases, the full hypermetropic correction will align the eyes for distance; however, a residual esotropia will persist at near. These patients have a high AC/A ratio, and bifocals are indicated (see Prescribing Bifocals below).

High AC/A Ratio Esotropia A subgroup of patients with accommodative esotropia will have a high AC/A ratio and have a signiﬁcantly larger esotropia at near. High AC/A ratio esotropia usually occurs in patients with hypermetropia but may occur in patients with myopia or no refractive error. If the eyes are straight in the distance (10 PD), a bifocal add is given to correct the near deviation and promote near fusion. Example 2. 4-year-old with esotropia for 2 months Full ductions and versions Cycloplegic refraction 3.50 OU

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With correction (cc) 4.00 OU Dcc E 4 (phoria—fusing) Ncc ET 25 Ncc with 3.00 add E 3 (phoria—fusing) Treatment: Prescribe bifocals (3.50 sphere upper with 3.00 add, OU)

Without correction (sc): Dsc ET 25 Nsc ET 55

PRESCRIBING BIFOCALS A bifocal add is indicated for patients who are fusing in the distance but have an esotropia at near that is large enough to interfere with near fusion (10 PD).42 The add will relax near accommodation, thus reducing convergence. If the AC/A ratio is 7 (high), then a 3.00 add will reduce the near esotropia by 21 PD. In the example above, the 3.00 add reduces the residual near deviation (with correction) to an esophoria of 3 PD, allowing for binocular fusion. Usually, start with a maximum near add of 3.00. Over time, the bifocal add can be diminished slowly to promote divergence. Reduce the reading add to produce a small esophoria of no more than 4 to 6 PD, which will stimulate divergence, while maintaining comfortable binocular fusion. In many cases, the bifocal can be eliminated by 10 to 12 years of age. The best bifocal is a ﬂat-top segment that bisects the pupil. A common mistake is to prescribe a low bifocal that a child can easily look over, thus negating the purpose of the bifocal add. Remember that bifocals will not treat a manifest esotropia in the distance. If a patient has an esotropia in the distance greater than 10 PD with full hypermetropic correction and is not fusing, then surgery is indicated, not bifocals. Bifocals, however, may be needed postoperatively if a near esotropia persists.

Partially Accommodative Esotropia If, after wearing full hypermetropic correction, a residual esotropia (10 PD) for distance and near exists, it is termed partially accommodative esotropia (Fig. 7-12C). The treatment is surgery: bilateral medial rectus muscle recessions. Example 3. 3-year-old with esotropia for 2 months Full ductions and versions Cycloplegic refraction 3.50 OU

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A

B FIGURE 7-12A–B. Infantile accommodative esotropia. The patient is the author’s youngest son who had partially accommodative esotropia. (A) At 6 weeks of age, the patient’s eyes were well aligned with normal motility. (B) At 3 months of age, a variable esotropia occurred. Deviation measured between essentially straight and an esotropia of 40 prism diopters.

Without correction (sc): Dsc ET 30 Nsc ET 35

With correction (cc) 3.50, OU: Dcc ET 20 Ncc ET 25

Treatment: Bilateral medial rectus recessions

C

D FIGURE 7-12C–D. (C) Cycloplegic refraction revealed a 5.50 refractive error OU. Patient was given full hypermetropic correction. However, a small residual esotropia persisted. In this photograph, note that the left eye is deviated and the Brückner reﬂex shows a brighter reﬂex in the left eye. Augmented surgery was performed at 6 months of age by the author. (D) Patient 3 years after surgery with straight eyes and excellent binocular function with stereoacuity as measured by Randot testing.

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E FIGURE 7-12E. (E) At the time of this writing, patient is 13 years old and is still well aligned with an excellent sensory outcome by Titmus stereoacuity testing showing a positive ﬂy and 3/3 animals (100 s).

After wearing the 3.50 sphere for 6 weeks, the patient in Example 3 still had a signiﬁcant esotropia (Dcc ET 20, Ncc ET 25). This residual esotropia cannot be fused and should be addressed surgically. Bifocals are not indicated, as they will not correct the distance deviation. Preoperatively, it is important to

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rerefract these patients to make sure that all full latent hypermetropia is corrected.

Surgery for Partially Accommodative Esotropia Bilateral medial rectus recession is the procedure of choice for partially accommodative esotropia. There is, however, controversy regarding how to determine the target angle. Most are now increasing the amount of surgery from the standard approach using augmented surgery or prism adaptation. Below are various formulas used to determine the amount of surgery for partially accommodative esotropia.

STANDARD SURGERY In Example 3, the standard surgery target angle is ET 20. The standard surgical approach has been to operate for the residual deviation measured with correction in the distance (i.e., standard surgery); however, standard surgery has a high undercorrection rate of approximately 25%. Because of this unacceptably high undercorrection rate, many surgeons are increasing their surgical numbers to correct partially accommodative esotropia. The idea of surgery is not to eliminate hypermetropic correction by overcorrection, but to get the eyes straight and fusing with full hypermetropic correction. Parents should be advised that spectacles will be required postoperatively.

AUGMENTED SURGERY This author has studied results using a target angle determined by averaging the near deviation with correction and the near deviation without correction. In Example 3, the augmented surgery target angle is 30 PD (35 25/2). Results comparing standard surgery to this augmented surgery formula showed a 26% undercorrection rate for standard surgery, while augmented surgery resulted in a 93% success rate with 7% overcorrection.70 The patients who were overcorrected all had a high AC/A ratio, were well aligned at near, and had an intermittent exotropia in the distance. The augmented surgery formula is based on the near measurement, so it is not surprising that patients with a high AC/A ratio have a tendency for overcorrection in the distance. This author augments surgery as described above if the AC/A ratio is normal; however, if the AC/A ratio is high, average the near deviation without correction (largest deviation) and the

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distance deviation with correction (smallest deviation), or use prism adaptation. The high AC/A ratio patients are difﬁcult to manage.

PRISM ADAPTATION Another method for determining the amount of surgical correction in patients with partially accommodative esotropia is using prism adaptation. Prism adaptation consists of prescribing baseout prism for the residual esotropia after prescribing full hypermetropic correction. In Example 3, the initial press-on prism would be 20 PD base-out. The patient returns in approximately 2 weeks after wearing the prisms. If the esotropia has increased, then the prisms are increased. This regimen continues at 1- to 2-week intervals until the deviation has stabilized. The surgeon operates on the full prism-adapted angle as determined by the press-on prisms. Operating on the larger adapted angle reduces the undercorrection rate. Results of a multicenter study on prism adaptation showed that standard surgery resulted in approximately 75% successful correction rate and operating on the prism-adapted angle resulted in an 85% success rate; however, the difﬁcult high AC/A ratio patients were excluded from the study.58 The disadvantage of prism adaptation is the cost and time involved with prescribing press-on prisms and reexamining the patient until the deviation stabilizes.

POSTOPERATIVE CARE Postoperative care is similar to that described for congenital esotropia. The goal is to achieve binocular fusion, as most patients with acquired strabismus have fusion potential. Patients who are aligned for distance, but have an esotropia greater than 8 to 10 PD at near, may be candidates for bifocals. The vast majority of patients will require hypermetropic correction after surgery. A small consecutive exotropia can be managed by reducing the plus of hypermetropic spectacles, but do not “cut the plus” more than 2.50 diopters as this results in instability of the angle. Large overcorrections are rare but when they occur, they must be managed by surgery.

Miotics In rare selected patients, miotic drops such as phospholine iodide (i.e., echothiophate iodide) may be indicated to treat

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accommodative esotropia. Miotics, such as phospholine iodide, are cholinesterase inhibitors and increase the effectiveness of locally released acetylcholine. Topical phospholine iodine has a parasympathomimetic effect on the iris sphincter and ciliary muscles, causing miosis and pharmacological accommodation. Acetylcholine released in the ciliary body will last longer and produce more accommodation for a given amount of innervational stimulation. Thus, miotics reduce the accommodative effort necessary to provide a clear retinal image and will reduce the amount of associated reﬂex convergence. When using miotics, it is preferable to start with a low dose of phospholine iodide, 0.03%, one drop every morning. If this dose is not sufﬁcient to correct the esotropia, the dose may be increased to twice a day or use phospholine iodide 0.125%. Miotics truly reduce the AC/A ratio and esotropia associated with hypermetropia. Miotics can be tried if the patient has a high AC/A ratio and has minimal hypermetropia. In most cases, however, bifocal spectacles are the treatment of choice. Another indication for the use of miotics is in children who cannot wear spectacles or contact lenses; this is most useful for short periods of time, perhaps during the summer months when children are swimming. Miotics are occasionally used as a diagnostic test to determine if an esotropia will respond to hypermetropic optical correction. If the miotics fail to correct the deviation, this would identify a nonaccommodative component. Unfortunately, the only way to know if spectacles will correct the deviation is to actually prescribe them.

ADVERSE EFFECTS OF MIOTICS Phospholine iodide, even when given topically, is systemically absorbed and will lower cholinesterase activity in the blood for several weeks,14 which is of signiﬁcant note for those patients who undergo general anesthesia with succinylcholine. Phospholine iodide prolongs the effect of the succinylcholine and may prolong respiratory paralysis after surgery. Succinylcholine should be avoided if phospholine iodide has been used within 6 weeks before surgery. Systemic side effects of miotics may include brow ache, headaches, nausea, and abdominal cramping. If the lower dose of phospholine iodide is used, these complications are infrequent. Ocular side effects of phospholine iodide include iris cysts along the pupillary margin in 20% to 50% of cases, occurring at

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any time from several weeks to several months after treatment. Iris cysts tend to regress after discontinuing phospholine iodide; however, this author has seen persistent iris cysts several years after stopping phospholine iodide therapy. Phenylephrine used in combination with phospholine iodide may prevent iris cysts. Other rare and unusual complications include lens opacities, retinal detachment in adults, and angle-closure glaucoma.

INFANTILE ACCOMMODATIVE ESOTROPIA Infantile accommodative esotropia occurs during the ﬁrst year of life. The key to diagnosing infantile accommodative esotropia is noting the presence of hypermetropia (2.00) and a variableangle esotropia at the onset.4,56 Treatment is to immediately prescribe the full hypermetropic correction, as determined by a good cycloplegic refraction, and treat amblyopia if present (see Fig. 7-11).18 If spectacles do not align the eyes to within 8 to 10 PD, then strabismus surgery is indicated (see Partially Accommodative Esotropia, discussed previously). The child should wear spectacles for at least 4 weeks before going to surgery. Approximately half of diagnosed patients will be corrected with spectacles alone, and half will require spectacles along with surgery (see Treatment of Partially Accommodative Esotropia, discussed previously). This author is personally very familiar with this disorder, as his youngest son developed partially accommodative esotropia that did not respond to full hypermetropic correction at 4 months of age. The author operated on his son at 6 months of age using the augmented surgery formula (Fig. 7-12). Now, at 13 years of age, he has done well with just the one surgery, having straight eyes and high-grade stereoacuity. The prognosis for binocular fusion in patients with accommodative esotropia is quite good, as these patients have acquired strabismus. The treatment goal for accommodative esotropia is establishing binocular fusion and stereopsis.

ACQUIRED NONACCOMMODATIVE ESOTROPIA Uncommonly, esotropia is acquired during childhood or even adulthood without signiﬁcant hypermetropia. Initially, these deviations are variable and intermittent. Over time (weeks,

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months, or even years), however, the esodeviation may become constant. It is important in these cases of acquired esotropia to rule out the possibility of an intracranial tumor, Arnold–Chiari malformation, or other neurological processes such as myasthenia gravis. A divergence paralysis pattern with a larger esotropia in the distance than at near is a red ﬂag to the possibility of a mild sixth nerve paresis and a neurological disorder. The treatment for acquired nonaccommodative esotropia is usually surgery, and the prognosis for re-establishing binocular fusion is relatively good. Undercorrections are frequent in this group, and prism adaptation will help reduce the number of patients with a residual esotropia.

ESOPHORIA Small esophorias (8–10 PD) can cause signiﬁcant asthenopic symptoms. These patients usually complain of headaches and fatigue when reading for long periods of time. Small esophorias are best treated with hypermetropic correction for near esophorias, or base-out prisms if the deviation is present for distance and near. A reading add relaxes accommodation and convergence, thus correcting the esophoria. Base-out prisms are very effective; however, patients tend to adapt to the prisms and require increasing prisms over time. When prescribing prisms, prescribe just enough for comfortable fusion but slightly less than the full deviation to stimulate divergence. In cases of a large esophoria, surgery may be required. In these cases, it is helpful to use prism adaptation to disclose the full underlying esophoria. In any case of a symptomatic esophoria, a cycloplegic refraction is indicated, as latent hypermetropia is a common cause for an acquired esodeviation.

ESOTROPIA, NYSTAGMUS, AND FACE TURN Nystagmus may occur with esotropia. These patients often adopt a face turn to damp the nystagmus and improve visual acuity. Speciﬁc types of esotropia, nystagmus, and face turn syndromes include (1) manifest latent nystagmus, (2) congenital nystagmus with constant esotropia, and (3) nystagmus compen-

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sation syndrome. In these cases, the face turn is used to position the ﬁxing eye at the null point to improve vision. In the case of manifest latent nystagmus and nystagmus compensation syndrome, the null point is always in adduction. Consequently, the ﬁxing eye in these cases is always adducted and the face turn is toward the side of the ﬁxing eye (Fig. 7-13). Ciancia’s syndrome (see Fig. 7-5 and Congenital Esotropia, discussed previously) is often placed in this category; however, the cause for the face turn is tight medial rectus muscles, not nystagmus and a null point.

FIGURE 7-13. Esotropia, nystagmus, and face turn. Drawing shows that the null point of the nystagmus is in adduction, so the patient adopts a face turn to the right to place the ﬁxing right eye in adduction. Note that the face turn is to the same side as the ﬁxing eye.

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Manifest Latent Nystagmus Latent nystagmus (see p. 225) that spontaneously becomes manifest without monocular occlusion is called manifest latent nystagmus. The null point for manifest latent nystagmus is always in adduction. Patients with strabismus and manifest latent nystagmus will place the ﬁxing eye in adduction to improve vision; this produces a face turn to the side of the ﬁxing eye.23 Patients with intermittent strabismus and latent nystagmus will not manifest the nystagmus when they are aligned and fusing. At these times, the patient has straight eyes or a microtropia and fusion, so the latent nystagmus is controlled, and there is no face turn. Other times (e.g., when the patient is fatigued), the phoria breaks down to a tropia and loss of fusion. Loss of peripheral fusion changes the latent nystagmus to a manifest latent nystagmus. This causes the patient to adopt a face turn to place the ﬁxing eye at the null point that is in adduction (Fig. 7-14). The treatment of manifest latent nystagmus with face turn is to enhance binocular fusion in order to avoid the tropia phase. Methods for enhancing binocular fusion in patients with esotropia include providing hypermetropic correction in patients with an accommodative component or operating for the residual esodeviation. In the article by Zubcov et al.,73 ﬁve patients with esotropia and manifest latent nystagmus underwent strabismus surgery resulting in straight eyes; this converted the manifest latent nystagmus to latent nystagmus. Four of the ﬁve patients also showed improvement in binocular visual acuity because of the improved nystagmus.

Congenital Nystagmus with Constant Esotropia Patients with congenital nystagmus may have an associated esotropia. These patients commonly adopt a face turn to place the ﬁxing eye at the null point. The null point in congenital nystagmus may be in any gaze position. If the null point is in adduction, with the right eye ﬁxing, the face turn will be to the right. Null point in abduction causes the ﬁxing eye to abduct, and then the face turn is to the left. A vertical null point position causes a compensatory chin depression or chin elevation. Obviously, there is no face turn if the null point is in primary position.

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A

B FIGURE 7-14A,B. Manifest latent nystagmus. Patient with Down’s syndrome and previous surgery for congenital esotropia. Patient now has an intermittent esotropia with peripheral fusion and monoﬁxation syndrome. (A) Patient is fusing with a microesotropia. There is an underlying latent nystagmus that is controlled because the patient is fusing. Note that there is no face turn. (B) Now the patient has esotropia, which disrupts fusion and changes the latent nystagmus into a manifest latent nystagmus. The null point of manifest latent nystagmus is in adduction, so the ﬁxing eye (the right eye) moves into adduction. The patient has developed a face turn to the right. Note the positive Brückner reﬂex with the brighter red reﬂex in the deviated left eye.

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Congenital nystagmus is a jerk, or pendular, nystagmus. The characteristics of congenital nystagmus are different from manifest latent nystagmus. With congenital nystagmus, there is an increasing velocity of the slow phase and no change in the nystagmus on unilateral occlusion or binocular dissociation. The nystagmus switches direction on sidegaze with the fast phase to the right in rightgaze and the fast phase to the left in leftgaze. Congenital nystagmus and latent, or manifest, nystagmus can occur concurrently. The treatment for the face turn with esotropia is strabismus surgery to move the null point of the ﬁxing eye to primary position. Then, if necessary, move the nonﬁxing eye to match. For example, if there is a right esotropia of 40 PD (20°), right eye ﬁxing in adduction with a face turn to the right 20° (see Fig. 7-13), recess the right medial rectus and resect the right lateral rectus; this will move the right eye to primary position and correct the face turn and the esotropia at the same time (also see Chapter 10).

Nystagmus Compensation Syndrome (Nystagmus Blockage Syndrome) Some patients with congenital nystagmus and straight eyes may use accommodative convergence to damp their nystagmus. In rare circumstances, this can produce an esotropia. Previously, this rare syndrome has been termed nystagmus blockage syndrome or nystagmus compensation syndrome.66 These patients present with straight eyes and congenital nystagmus. On viewing near targets, they manifest a variable esodeviation while using accommodative convergence to damp the nystagmus and improve vision. Key observations include variable-angle intermittent esotropia only at near, and pupillary miosis that occurs with the esotropia (Fig. 7-15). Many patients who have been previously reported in the literature as having nystagmus blockage syndrome or nystagmus compensation syndrome actually had manifest latent nystagmus. Some have doubted the existence of congenital nystagmus with accommodative convergence causing esotropia; however, von Noorden66 has documented this syndrome with EOG recordings. Currently, a good surgical treatment for this esotropia at near does not exist. However, von Noorden has suggested a small medial rectus recession with Faden (posterior ﬁxation suture).

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A

B FIGURE 7-15A,B. (A) Nystagmus compensation syndrome. Top photograph: patient with congenital nystagmus, straight eyes, and middilated pupils. Bottom photograph: patient trying to read a near target. When patient tries to read the near target, the patient invokes accommodative convergence to damp the nystagmus and an esotropia occurs. Visual acuity improves to 20/40 at near. (Photograph courtesy of G.K. von Noorden.) (B) Electro-oculograph of a patient with congenital nystagmus and nystagmus compensation syndrome. At the beginning of the tracing, the congenital nystagmus shows large amplitude and visual acuity is 20/100. The patient then uses accommodative convergence to damp the nystagmus, an esotropia occurs, and visual acuity improves to 20/40 at near. The amplitude of the nystagmus increases as patient relaxes accommodative convergence and the congenital nystagmus recurs. (From Ref. 67, with permission.)

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CYCLIC ESOTROPIA Cyclic esotropia is a very rare type of esotropia, with most pediatric ophthalmologists only seeing one or two cases in their entire career. This is an acquired esotropia that occurs at virtually any age, but most frequently between 2 and 6 years of age. These patients usually cycle between straight eyes and esotropia every 24 to 48 h; however, the interval may vary. To help establish a pattern, ask the parents to record on a calendar when the eyes are crossed versus the days when the eyes are straight. When the eyes are aligned, the patient has good binocular vision and stereoacuity. Cyclic esotropia is usually progressive and, in most cases, the esodeviation ﬁnally becomes constant over several months to years. Some cases of cyclic esotropia are associated with hypermetropia and, in these cases, the full cycloplegic correction should be given. Patients in whom there is no signiﬁcant hypermetropia, surgery for the full deviation should be performed to provide appropriate eye alignment and preserve binocularity and fusion.13,29 Sporadic cases associated with sixth nerve palsy or central nervous system disease have also been reported.34,54

DIVERGENCE INSUFFICIENCY Divergence insufﬁciency causes an esodeviation that is greater in the distance than at near and can occur, idiopathically, as a primary strabismus. An important cause for divergence insufﬁciency is divergence paralysis secondary to a mild sixth nerve palsy that causes an esodeviation in the distance. An acquired esodeviation with a divergence paresis pattern is a red ﬂag for possible neurological disease. Divergence paresis has been associated with pontine tumor, head trauma, myasthenia gravis, and Arnold–Chiari malformation. Neuroimaging studies as well as a neurological consultation are indicated to rule out possible neurological disease.

SENSORY ESOTROPIA Sensory esotropia is an esotropia occurring secondary to unilateral blindness. It has been the general teaching that, if the vision loss occurred before 2 years of age, the patient will develop

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esotropia and, after 2 years of age, will develop exotropia. This theory has not been borne out, however, as many infants with unilateral visual loss develop exotropia. Surgery for sensory esotropia is a recession of the medial rectus muscle and a resection of the lateral rectus muscle of the blind eye.

References 1. Aiello A, Wright KW, Borchert M. Independence of optokinetic nystagmus asymmetry and binocularity in infantile esotropia. Arch Ophthalmology 1994;112:1580–1583. 2. Archer SM, Sondhi N, Helveston EM. Strabismus in infancy. Ophthalmology 1989;96:133–137. 3. Arthur BW, Smith JT, Scott WE. Long-term stability of alignment in the monoﬁxation syndrome. J Pediatr Ophthalmol Strabismus 1989;26:224–231. 4. Baker JD, Parks MM. Early onset accommodative esotropia. Am J Ophthalmol 1980;90:11. 5. Birch E, Stager D, Wright K, Beck R. The natural history of infantile esotropia during the ﬁrst six months of life. J AAPOS 1998;2:325– 329. 6. Birch EE, Gwiazda J, Held RR. Stereo acuity development of crossed and uncrossed disparities in human infants. Vision Res 1982;22:507. 7. Birch EE, Petrig BL. FPL and VEP measures of fusion, stereopsis, and stereo acuity. Technical digest series. Noninvasive assessment of the visual system. Washington, DC: Optical Society of America, 1994. 8. Birch EE, Stager DR, Berry P, Everett ME. Prospective assessment of acuity and stereopsis in amblyopic infantile esotropes following early surgery. Investig Ophthalmol Vis Sci 1990;31:758–765. 9. Birch EE, Stager DR, Everett ME. Random dot stereo acuity following surgical correction of infantile esotropia. J Pediatr Ophthalmol Strabismus 1995;32:231–235. 10. Birch EE, Stager DR. Monocular acuity and stereopsis in infantile esotropia. Invest Ophthalmol Vis Sci 1985;26:1624–1630. 11. Birch E, Fawcett S, Stager DR. Why does early surgical alignment improve stereo acuity outcomes in infantile esotropia? J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(1):10–14. 12. Braddick O, et al. Cortical binocularity in infants. Nature (Lond) 1980;288:363–365. 13. Cahill M, Walsh J, McAleer A. Recurrence of cyclic esotropia after surgical correction. J Am Assoc Pediatr Ophthalmol Strabismus 1999;3(6):379–380. 14. Chin NV, Gold AA, Breinin GM. Iris cysts and miotics. Arch Ophthalmol 1964;71:611. 15. Ciancia A. La esotropia en el lactante, diagnostico y tratamiento. Arch Chil Oftalmol 1962;9:117.

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16. Clarke WN, Noel LP. Vanishing infantile esotropia. Can J Ophthalmol 1982;17:100–102. 17. Clarke WN. Current controversies: very early vs. early or late surgery for infantile esotropia. Can J Ophthalmol 1995;30:239–240. 18. Coats DK, Avilla CW, Paysse EA, Sprunger DT, Steinkuller PG, Somaiya M. Early-onset refractive accommodative esotropia. J Am Assoc Pediatr Ophthalmol Strabismus 1998;2(5):275–278. 19. Costenbader FD. Infantile esotropia. Trans Am Ophthalmol Soc 1961;59:397. 20. Crawford ML, Harwerth RS, Smith EL, von Noorden GK. Loss of stereopsis in monkeys following prismatic binocular dissociation during infancy. Behav Brain Res 1996;79(1–2):207–218. 21. Crawford MLJ, von Noorden GK. Optically induced concomitant strabismus in monkeys. Investig Ophthalmol Vis Sci 1980;19:1105. 22. Crawford MLJ, von Noorden GK. The effects of short-term experimental strabismus on the visual system in Macaca mulatta. Investig Ophthalmol Vis Sci 1979;18:496–505. 23. Dell’Osso LF, Ellenberger C Jr, Abel LA, Flynn JT. The nystagmus blockage syndrome. Investig Ophthalmol Vis Sci 1983;24:1580. 24. Dickey CF, Metz HS, Stewart SA. The diagnosis of amblyopia in cross-ﬁxation. J Pediatr Ophthalmol Strabismus 1991;28:171–175. 25. Fawcett S, Lefﬂer J, Birch EE. Factors inﬂuencing stereoacuity in accommodative esotropia. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(1):15–20. 26. Fox R, et al. Stereopsis in human infants. Science 1980;207:323. 27. Friedrich D, de Decker W. Prospective study of the development of strabismus during the ﬁrst 6 months of life. Orthopt Hor 1987: 21–28. 28. Helveston EM, Ellis FD, Schott J, et al. Surgical treatment of congenital esotropia. Am J Ophthalmol 1983;96:218–228. 29. Helveston EM. Cyclic strabismus. Am Orthopt J 1971;23:4851. 30. Helveston EM, Neely DF, Stidham DB, Wallace DK, Plager DA, Sprunger DT. Results of early alignment of congenital esotropia. Ophthalmology 1999;106:1716–1726. 31. Hiles DA, Watson BA, Biglan AW. Characteristics of infantile esotropia following early bimedial rectus recession. Arch Ophthalmol 1980;98:697–703. 32. Hoyt C, Jastrzebski G, Marg E. Amblyopia and congenital esotropia. Visually-evoked potential measurements. Arch Ophthalmol 1984; 102:58–61. 33. Hubel DH, Wiesel TN. Binocular interaction in striate cortex of kittens reared with artiﬁcial squint. J Neurophysiol 1965;28:1041– 1059. 34. Hutcheson KA, Lambert SR. Cyclic esotropia after a traumatic sixth nerve palsy in a child. J Am Assoc Pediatr Ophthalmol Strabismus 1998;2(6):376–377. 35. Ing MR. Early surgical alignment for congenital esotropia. Trans Am Ophthalmol Sci 1981;79:625–663.

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36. Ing M, Costenbader FD, Parks MM. Early surgical treatment for congenital esotropia. Am J Ophthalmol 1966;652:1419–1427. 37. Ing MR. Progressive increase in the angle of deviation in congenital esotropia. Trans Am Ophthalmol Soc 1994;XCII:117–259. 38. Ing MR. Botulinum alignment for congenital esotropia. Ophthalmology 1993;100(3):318–322. 39. Ing MR. Outcome study of surgical alignment before six months of age for congenital esotropia. Ophthalmology 1995;102:2041–2045. 40. Ing MR. Outcome study of stereoacuity in relation to duration of misalignment in congenital esotropia. JAAPOS 2001;Feb.6(1):3–8. 41. Leguire LE, Roger GL, Bremer DL. Visual-evoked response binocular summation in normal and strabismic infants. Investig Ophthalmol Vis Sci 1991;32:126–133. 42. Ludwig IH, Parks MM, Getson PR. Long-term results of bifocal therapy for accommodative esotropia. J Pediatr Ophthalmol Strabismus 1989;26:264–270. 43. Magoon E. Chemodenervation of strabismic children. Ophthalmology 1989;96:931–934. 44. Maumenee IH, Alston A, Mets MB, Flynn JT, Mitchell TN, Beaty TH. Inheritance of congenital esotropia. Trans Am Ophthalmol Soc 1986;84:85–93. 45. Mohoney BG, Erie JC, Hodge DO, Jacobsen SJ. Congenital esotropia in Olmsted County, Minnesota. Ophthalmology 1998;105:846–850. 46. Morris RJ, Scott WE, Dickey CF. Fusion after alignment of longstanding strabismus in adults. Ophthalmology 1993;100:135–138. 47. Mutti DO, Frane SL, Friedman NE, Lin WK, Sholtz RI, Zadnik K. Ocular component changes during emmetropization in infancy (abstract). Investig Ophthalmol Vis Sci 2000;41:S300. 48. Nelson LB, Wagner RS, Simon JW, Harley RD. Congenital esotropia. Surv Ophthalmol 1987;31:363–383. 49. Nixon RB, Helveston EM, Miller K, Archer SM, Ellis FD. Incidence of strabismus in neonates. Am J Ophthalmol 1985;100:798–801. 50. Parks MM. Congenital esotropia with a bi-ﬁxation result: report of a case. Doc Ophthalmol 1984;58:109–114. 51. Pediatric Eye Disease Investigator Group. The clinical spectrum of early-onset esotropia. Experience of the Congenital Esotropia Observational Study. Am J Ophthalmol 2002;133:102–108. 52. Pediatric Eye Disease Investigator Group. Spontaneous resolution of early-onset esotropia: experience of the Congenital Esotropia Observational Study. Am J Ophthalmol 2002;133:109–118. 53. Petrig B, Juless B, Kropff W, Baumgartner G, Anliker M. Development of stereopsis and cortical binocularity in human infants: electrophysiological evidence. Science 1981;213:1402–1405. 54. Pillai P, Dhand UK. Cyclic esotropia with central nervous system disease: report of two cases. J Pediatr Ophthalmol Strabismus 1987;24(5):237–241. 55. Podgor MJ, Remaley NA, Chew E. Associations between siblings for esotropia and exotropia. Arch Ophthamol 1996;114:739–744.

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56. Pollard ZF. Accommodative esotropia during the ﬁrst year of life. Arch Ophthalmol 1976;94:1912. 57. Prieto-Diaz J. Large bilateral medial rectus recession in early esotropia with bilateral limitation of abduction. J Pediatr Ophthalmol Strabismus 1980;17:101–105. 58. Prism Adaptation Research Group. Efﬁcacy of prism adaptation in the surgical management of acquired esotropia. Arch Ophthalmol 1990;108:1248–1256. 59. Robb RM, Rodier DW. The variable clinical characteristics and course of early infantile esotropia. J Pediatr Ophthalmol Strabismus 1987;24:276–281. 60. Scott WE. Temporary surgical overcorrection of infantile esotropia. Transactions of the New Orleans Academy of Ophthalmology. New York: Raven Press, 1986. 61. Shauly Y, Prager TC, Mazow ML. Clinical characteristics and longterm postoperative results of infantile esotropia. Am J Ophthalmol 1994;117:183–189. 62. Shirabe H, Mori Y, Dogru M, Yamamoto M. Early surgery for infantile esotropia. Br J Ophthalmol 2000;84:536–538. 63. Smith JT, Scott WE. Long-term stability of alignment in the monoﬁxation syndrome. J Pediatr Ophthalmol Strabismus 1989;Sep.–Oct. 26(5):224–231. 64. Sondhi N, Archer S, Helveston EM. Development of normal ocular alignment. J Pediatr Ophthalmol Strabismus 1988;25:210. 65. Tychsen L, Lisberger SG. Maldevelopment of visual motion processing in humans who had strabismus with onset in infancy. J Neuroci 1986;6:2495–2508. 66. von Noorden GK. The nystagmus compensation (blockage syndrome). Am J Ophthalmol 1976;82:283. 67. von Noorden GK, Munoz M, Wong SY. Compensatory mechanisms in congenital nystagmus. Am J Ophthalmol 1987;104:387–397. 68. Wilson ME, Parks MM. Primary inferior oblique overaction in congenital esotropia, accommodative esotropia, and intermittent exotropia. Ophthalmology 1989;96:950–955. 69. Wright KW. Clinical optokinetic nystagmus asymmetry in treated esotropes. J Pediatr Ophthalmol Strabismus 1996;33(3):153–155. 70. Wright KW, Bruce-Lyle L. Augmented surgery for esotropia associated with high hypermetropia. J Pediatr Ophthalmol Strabismus 1993;30:167–170. 71. Wright KW, Edelman PM, McVey JH, Terry AP, Lin M. High-grade stereoacuity after early surgery for congenital esotropia. Arch Ophthalmol 1994;112:913–919. 72. Wright KW, Edelman PM, Walonker F, Yiu S. Reliability of ﬁxation preference testing in diagnosing amblyopia. Arch Ophthalmol 1986; 104:549. 73. Zubcov AA, Reinecke RD, Gottlob I, Manley DR, Calhoun JH. Treatment of manifest latent nystagmus. Am J Ophthalmol 1990;110:160– 167.

8 Exotropia Kenneth W. Wright

E

xodeviations are quite common, and they are not necessarily pathological. A small intermittent exotropia is normal in most newborns, as 70% of normal newborns have a transient exodeviation that resolves by 2 to 4 months of age.1 Another type of exodeviation that is considered normal is a small exophoria, usually less than 10 prism diopters (PD). Most normal adults have a small exophoria when fully dissociated. Exodeviations are controlled with our innate strong fusional convergence, typically measuring 30 PD or more. The most common form of divergent strabismus is intermittent exotropia, which probably accounts for more than 90% of all exodeviations. Table 8-1 lists the different categories of pathological exodeviations, with the one most frequently occurring listed ﬁrst.

INTERMITTENT EXOTROPIA Intermittent exotropia is a large phoria that is intermittently controlled by fusional convergence. Unlike a phoria, intermittent exotropia spontaneously breaks down into a manifest exotropia (Fig. 8-1).

Clinical Features Intermittent exotropia is usually ﬁrst observed by the parents in early childhood or late infancy as an infrequent drifting or squinting of one eye. 12 Patients with intermittent exotropia tend to manifest their deviation when they are tired, have a cold or the ﬂu, or when they are daydreaming. Adult patients will often become exotropic after imbibing alcoholic beverages or taking sedatives. 266

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TABLE 14.1. Classiﬁcations of Exodeviations. Intermittent exotropia (common) Convergence insufﬁciency (common) Sensory exotropia (common) Congenital exotropia (rare)

Signs of intermittent exotropia include blurred vision, asthenopia, visual fatigue, and, rarely, diplopia in older children and adults. Many patients with intermittent exotropia have photophobia (squinting to bright light). Photophobia was originally thought to be a way for eliminating diplopia or confusion, but Wiggins and von Noorden have shown that the photophobia may not be related to diplopia avoidance.39 As a rule, during the phoric phase of intermittent exotropia, the eyes are perfectly aligned and the patient has bifoveal fusion with excellent stereoacuity ranging between 40 and 50 s arc. This excellent bifoveal fusion develops because the eyes are well aligned in early infancy when the critical binocular cortical connections are being established. A minority of patients with intermittent exotropia are primary monoﬁxators and do not develop normal bifoveal fusion with good stereopsis. Rarely a patient will even have signiﬁcant amblyopia. The poor fusion in these cases is associated with a predominance of the tropia phase. During the tropia phase of intermittent exotropia, patients will show large hemiretinal or regional suppression of the temporal retina.26,30 Anomalous retinal correspondence in the tropia phase and normal retinal correspondence in the phoria phase have been demonstrated in some patients with intermittent exotropia.4,38

Natural History The natural history of intermittent exotropia remains obscure, as there are no longitudinal prospective studies and only a few retrospective studies of untreated intermittent exotropia. Von Noorden found that 75% of 51 untreated patients showed progression over an average follow-up period of 3.5 years, whereas 9% worsened and 16% improved.36,38 Hiles et al.,20 in their study of 48 patients, found no signiﬁcant change in the deviation after an average of 11 years follow-up, and 2 patients progressed to a constant tropia. The most we can say about the natural history is that, in the majority of cases, intermittent exotropia does not get better; it either stays the same or progresses. If the tropic phase increases, patients may develop dense suppression and,

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A

B FIGURE 8-1A–B. (A) Patient with intermittent exotropia and straight eyes in the phoric phase. Patient has 40 s arc stereoacuity. (B) Occlusion of the right eye disrupts fusion and manifests the exotropia. Under the occluder, the right eye is deviated temporally.

over time, may progress to a constant exotropia with loss of fusional potential.

Classiﬁcations Intermittent exotropia has been classically categorized into three subtypes based on the difference between the distance

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C FIGURE 8-1C. (C) Occluder is removed and the right eye is deviated temporally, showing the exotropia. Patient is in the tropic phase and suppresses right eye.

deviation and the near deviation. These three “older” classic categories are (1) basic, (2) pseudodivergence excess, and (3) true divergence excess. It is important to note that the older terminology uses the term divergence excess, and pseudodivergence excess is only descriptive as to the difference of the deviation distance versus near; it is not meant to imply a mechanism for the distance–near disparities. The mechanism for the distance–near disparities seen in patients with intermittent exotropia is most likely caused by superimposed overconvergence on the basic exodeviation. These convergence mechanisms include tonic fusional convergence (tenacious proximal fusion),22 accommodative convergence (AC/A ratio), and proximal convergence (instrument convergence).

BASIC INTERMITTENT EXOTROPIA With this type of exotropia, there is no signiﬁcant distance–near disparity, and the distance deviation is within 10 PD of the near deviation. Patients with a basic deviation have normal convergence, so their deviation is essentially the same for distance and near.

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PSEUDODIVERGENCE EXCESS This is an exodeviation that is measured larger for distance ﬁxation than near ﬁxation by brief alternate cover testing (distance 10 PD greater than near); however, with prolonged monocular occlusion (patch test for 30–60 min), the near deviation increases and becomes similar to the distance deviation (within 10 PD). For example, an exodeviation measures 30 PD in the distance and 10 PD at near to alternate cover testing. One eye is patched for 30 min, and now the patient measures 30 PD in the distance and 25 PD at near. This change occurs because patients with pseudodivergence excess have increased tonic near fusional convergence that dissipates slowly after monocular occlusion. Prolonged monocular occlusion of 30 to 60 min is required in these patients to dissipate tonic near fusional convergence and disclose the full latent deviation (see Patch Test, below). The relatively brief period of monocular occlusion that occurs with alternate cover testing is not enough to break up the tonic near fusional convergence and disclose the full deviation at near. Surgery is performed for the full distance deviation. Pseudodivergence excess is quite common. More than 80% of patients with an apparent divergence excess actually have pseudodivergence excess, as the near deviation will increase to within 10 PD of the distance deviation after the patch test.5,22,37

PATCH TEST (OCCLUSION TEST) The patch test consists of placing an occlusive patch over one eye for at least 30 to 60 min, then measuring the deviation without letting the patient restore binocular fusion. The idea is to totally suspend all tonic fusional convergence by occluding one eye, forcing the full latent deviation to become manifest. When performing the patch test, be sure the patient does not peek around the patch and regain fusion before the deviation is measured. To measure the deviation, ﬁrst cover the unpatched eye with a paddle occluder, then remove the patch and measure the deviation with alternate cover testing. This method ensures the patient will not sneak a peek with both eyes and reestablish fusion before the deviation is measured.

TRUE DIVERGENCE EXCESS In these cases, the distance deviation is greater than the near deviation by more than 10 PD, even after performing the patch

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test. For example, the distance deviation would measure 30 PD, near deviation 10 PD and, after a 30-min patch test, the distance deviation would be 30 PD and the near deviation 15 PD. This author and Eugene De Juan (Los Angeles, CA) studied the cause of true divergence excess at the Wilmer Clinic at Johns Hopkins Hospital in Baltimore in 1981. They found that most of the patients with true divergence excess had a high AC/A (accommodative convergence/accommodation) ratio as determined by a 3.00 add after a 60-min patch test. The patch test relaxes tonic fusional convergence, and the 3.00 add relaxes accommodation. The high AC/A ratio patients do not show an increase in the near exotropia to the patch test, but the near deviation increases dramatically with a 3.00 near add.40 In a similar study, Kushner22 found approximately 60% of patients with a true divergence excess had a high AC/A ratio and 40% had a normal AC/A ratio. The group with a high AC/A ratio was prone to postoperative overcorrection (75% overcorrection) at near if the distance measurement is used as the surgical target angle. The 40% of true divergence excess patients with a normal AC/A ratio had relatively good results using the distance measurement. Patients with true divergence excess are a difﬁcult group to surgically correct as they are prone to having a consecutive esotropia at near, and some will require bifocals or additional surgery. Following is a summary of the causes of overconvergence that produce true divergence excess.

CAUSES OF TRUE DIVERGENCE EXCESS HIGH AC/A RATIO This condition occurs when the distance deviation is larger than the near deviation even after the patch test, but the near deviation increases close to the distance deviation with a 3.00 add. High AC/A ratio intermittent exotropia has normal tonic fusional convergence but has a high AC/A ratio that causes the distance–near disparity. Surgery is usually performed for a deviation somewhere between the distance and near deviation measured without near add. Some of these patients require bifocals after surgery if there is an esotropia at near.

INCREASED PROXIMAL CONVERGENCE This situation arises when the distance deviation is larger than the near deviation after the patch test and a 3.00 add OU. These patients have a normal tonic fusional convergence and a

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normal AC/A ratio, but have increased proximal convergence that reduces the near deviation. Proximal convergence is independent of binocular fusion. Surgery should be performed for an angle between the distance and near deviation.

MIXED CONVERGENCE MECHANISM There are many cases where more than one mechanism of convergence causes the distance–near disparity. This group with mixed convergence mechanism explains the patients that do not speciﬁcally ﬁt into the pure categories listed previously. An example of a mixed convergence mechanism is when the distance deviation is 45 PD and the near deviation is 20 PD. After the patch test, the near deviation increases to 30 PD and, with a 3.00 near add and the patch test, the near deviation equals the distance. In this example, there is a component of increased tonic fusional convergence brought out by the patch test and a slightly high AC/A ratio (AC/A ratio 5; i.e., 45 30/3.00) disclosed by the 3.00 add. Both the increased tonic fusional convergence and the slightly high AC/A ratio contribute to the distance–near disparity. Surgery is performed for the angle measured between the distance deviation and near the deviation (after the patch test).

Measuring the Exodeviation Obtaining reproducible measurements in a patient with intermittent exotropia can be difﬁcult, as the angle of deviation is often variable when measured by routine alternate cover prism testing. If it is late in the day and the patient is tired, fusional convergence will be weak and a large deviation will be easily manifest. On the other hand, if the patient is wide awake and alert, strong fusional convergence will keep the deviation small and difﬁcult to elicit. The patch test reduces variability secondary to fusional convergence because prolonged monocular occlusion disrupts fusion and discloses the full latent deviation. Because most patients with intermittent exotropia often have strong tonic fusional convergence, they should be measured using prolonged alternate cover testing, making sure that one eye is always covered. If there is signiﬁcant angle variability or a signiﬁcant distance–near discrepancy after prolonged alternate cover testing, then a patch test is indicated. In contrast, patients who show consistent measurements and no signiﬁcant distance near disparity do not need the patch test.

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FAR DISTANCE TEST Another technique that reduces measurement variability by disclosing the full distance deviation is the far distance test. This test is performed by simply having the patient ﬁxate on an object well past 20 feet to relax all proximal convergence. It is preferable to measure the deviation while the patient ﬁxates out a window to a far distant target. Combining the patch test and the far distance test has greatly reduced undercorrections and has improved overall results.

Treatment of Intermittent Exotropia NONSURGICAL TREATMENT In general, nonsurgical treatments for intermittent exotropia are not very effective. One method is to prescribe 2 to 3 diopters of myopic correction over what is required by cycloplegic refraction.8 Overminusing induces accommodative convergence, thus reducing the exodeviation. Another method is part-time monocular occlusion therapy.15,18 By occluding the dominant eye, the patient is forced to use the nonpreferred eye, thus providing antisuppression therapy. Although others have found success with this procedure, in this author’s experience, only a few patients have responded to this therapy. In virtually every case, the intermittent exotropia returns when the patching is stopped. Part-time occlusion therapy may be tried in younger patients as a method for delaying surgery, but it is only a temporary measure. Convergence exercises are useful for convergence insufﬁciency but not for most cases of intermittent exotropia. The use of antisuppression orthoptic therapy and diplopia awareness are not indicated, as this practice may lead to intractable diplopia and is detrimental to the patient.

INDICATIONS FOR SURGERY As with any strabismus, the indications for surgery include preservation or restoration of binocular function and cosmesis. In intermittent exotropia, one of the most important indications for therapeutic intervention is an increasing tropia phase. If the frequency or duration of the tropia phase increases, this indicates diminished fusional control and a potential for loss of binocularity. Progression should be monitored by recording size, frequency, duration of the exotropia, and the ease of dissociation

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after brief monocular occlusion. Documentation of deteriorating fusional control is an indication for treatment. Additionally, if the exotropia is manifest more than 50% of waking hours, surgery is probably indicated. In most cases, surgery should be delayed until 4 years of age. A study comparing surgery performed at various ages showed a signiﬁcant increase in the incidence of amblyopia and loss of stereopsis when a consecutive esotropia occurred in children under 4 years of age.14 Because the desired result is an initial consecutive esotropia, younger children who have surgery for intermittent exotropia are at risk for developing amblyopia and losing binocularity. If, however, the exotropia is present more than 50% of waking hours, and is increasing in size, frequency, or duration, then early surgery may be indicated even in children under 4 years of age. Richard and Parks32 found no signiﬁcant difference in results between early or late surgery, and Pratt-Johnson et al.29 actually had better results when surgery was performed under 4 years of age. The take-home message is that patients can be operated safely under 4 to 6 years of age for intermittent exotropia, but they must be followed closely, because a persistent consecutive esotropia can cause loss of stereopsis and amblyopia in this age group.

SURGICAL TREATMENT CHOICE

OF

PROCEDURE

For all three classic types of intermittent exotropia (i.e., basic, pseudodivergence excess, and true divergence excess), bilateral lateral rectus recessions work well. Symmetrical surgery is usually preferred over a monocular resect/recess procedure, as recession/resection procedures produce lateral incomitance with a signiﬁcant esotropia in the side of the operated eye. This incomitance can produce diplopia in sidegaze that may persist for months or even years. In patients with amblyopia of 20/50 or worse, a recession/resection procedure on the amblyopic eye is preferred, avoiding surgery on the “good” eye.

ROLE

OF THE

PATCH TEST

Historically, the patch test was important to distinguish among the three subgroups of intermittent exotropia because patients with basic or pseudodivergence intermittent exotropia would receive a monocular recess/resect procedure, whereas patients with true divergence excess would undergo bilateral lateral

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28

rectus recessions. Parks has shown that bilateral lateral rectus recessions work well for all three types of intermittent exotropias, so the patch test is probably not very important for determining whether a recess/resect or a bilateral recession should be performed. The patch test is, however, very useful in patients with a distance–near disparity to bring out the full deviation. Use the patch test in divergence excess cases to determine if there is pseudo- or true divergence excess.

AMOUNT

OF

SURGERY

Surgical parameters for patients with basic or pseudodivergence excess intermittent exotropia should be based on the full distance deviation as determined by alternate cover testing or the patch test. Patients with true divergence excess, however, should be treated more conservatively, especially if there is an associated high AC/A ratio. These patients are difﬁcult to manage, because totally correcting the distance deviation often leads to a persistent esotropia at near that may require postoperative bifocal glasses.22 If a true divergence excess associated with a high AC/A ratio is present, it is best to operate for a deviation somewhere between the distance and near deviations. These patients with true divergence excess and a high AC/A ratio should be told they have a signiﬁcant risk for a persistent overcorrection and, postoperatively, may require a reoperation, a bifocal add, or miotic drops. Moore25 suggested reducing the amount of recession in patients with lateral incomitance. It is this author’s experience that even moderate amounts of lateral incomitance are not important.

A- AND V-PATTERNS: OBLIQUE OVERACTION Intermittent exotropia may be associated with A- and V-patterns and inferior and superior oblique overaction (see Chapter 9). In these cases, it is appropriate to simultaneously operate on the obliques if dysfunction is present, or vertically offset the horizontal muscles for A- and V-patterns. Inferior oblique weakening procedures are safe in patients with bifoveal fusion and intermittent exotropia, but beware of performing superior oblique tenotomies or tenectomies, as this may result in a consecutive superior oblique paresis with intractable cyclovertical diplopia.41 If signiﬁcant superior oblique overaction and an “A” pattern is present, consider an infraplacement of the lateral

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rectus muscles or the Wright superior oblique tendon expander procedure, rather than a tenotomy or tenectomy of the superior oblique muscle. Do not signiﬁcantly alter the amount of horizontal surgery just because simultaneous oblique surgery is also being performed. Small vertical deviations associated with intermittent exotropia should be ignored, as these small vertical deviations usually disappear after surgery. Patients with large-angle intermittent exotropia may have an X-pattern, with the exotropia increasing in upgaze and downgaze relative to the deviation in primary position. In some cases, there is true overaction of all four oblique muscles; however, usually this pattern is due to tight lateral rectus muscles causing a leash effect similar to Duane’s syndrome upshoot and downshoot. The X-pattern is usually small, and it is best to address the pattern by simply performing bilateral lateral rectus recessions for the deviation in primary position.

POSTOPERATIVE CARE Immediately after surgery, a small consecutive esotropia of 8 to 10 PD is desirable, as even a large consecutive esotropia up to 20 PD may resolve without further surgery.31,33 Be sure to warn the parents and patients before surgery that postoperative diplopia may occur so they are not surprised. Postoperative diplopia associated with the initial overcorrection usually resolves by 1 to 2 weeks. In children under 4 years of age, alternate part-time patching of each eye helps prevent suppression and amblyopia and may facilitate straightening of the eyes. If a residual esotropia persists past 2 to 3 weeks, then the patient should be treated with prism glasses to neutralize the esotropia and re-establish fusion.17 Prescribe just enough prism to alleviate the diplopia, but leave a small residual esophoria to encourage divergence. If after 6 to 8 weeks the esotropia persists, then a reoperation should be considered. Advancement of the lateral rectus muscle is indicated if there is limited adduction or lateral incomitance that is consistent with a slipped muscle. Otherwise, bimedial recessions are usually the procedure of choice for a consecutive esotropia, especially if the esotropia is greater at near. If the consecutive esotropia is present only at near, one may consider a bifocal add, miotics, or even a base-out prism to correct the near esotropia while creating a small exodeviation in

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the distance. Failing this, small bimedial rectus recessions is the next option, with or without a Faden procedure. Patients with a residual exotropia greater than 10 PD after the ﬁrst postoperative week will probably not improve and most will require additional surgery. It is best to wait 8 weeks before reoperating on the residual exotropia. Rerecess both lateral rectus muscles if the primary surgery was bilateral recessions of 6.0 mm or less. If the primary recessions were greater than 6.0 mm, perform bilateral resections but be conservative, as overcorrections are common after resecting against a large recession.

PROGNOSIS The success rate, as in most types of strabismus, is dependent on the length of follow-up and, the longer the follow-up, the higher the incidence of undercorrection. Richard and Parks,32 in one of the longest follow-up studies, found a 56% success rate with one surgery, deﬁning success as a postoperative deviation less than 10 PD, with a follow-up period of 2 to 8 years (mean, 4 years). Thirty-eight percent (38%) of their patients were undercorrected and 6% were overcorrected. An additional surgery improved their success rate to just over 80%. Hardesty16 reported an 80% success rate after no more than two surgeries with a 10-year follow-up. Hardesty attributed the long-term success to the aggressive use of postoperative prisms for both over- and undercorrections to maintain constant fusion to prevent suppression.

CONVERGENCE INSUFFICIENCY Convergence insufﬁciency is the inability to maintain convergence on objects as they approach from distance to near. Symptoms usually ﬁrst occur during the teenage years and include asthenopia, reading difﬁculty, blurred near vision, and diplopia. Alternate cover testing will disclose a near exophoria with essentially no distance deviation. The exophoria at near intermittently breaks down into a tropia, especially after prolonged near work such as reading. When tropic, most patients will see double while some will not, as they have learned to suppress. Even patients with suppression can experience asthenopia and are often symptomatic.

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Patients with convergence insufﬁciency will show a remote near point of convergence. The near point of convergence (NPC) is how close one can bring a ﬁxation target to the nose and still maintain fusion. The break point is when the target is too close, fusion breaks, and an exotropia becomes manifest. The normal NPC is between 5 to 10 cm from the bridge of the nose. Patients with convergence insufﬁciency will have a remote break point ranging from 10 to 30 cm or more. Convergence insufﬁciency may also be associated with reduced fusional convergence amplitudes. Normal fusional convergence amplitudes for near are between 30 to 35 PD, but patients with convergence insufﬁciency usually break with less than 20 PD base-out. Some patients with convergence insufﬁciency will initially show a fairly good near point of convergence and convergence fusion amplitudes at near; however, on repeat testing, they are easily fatigued. The diagnosis of convergence insufﬁciency should not be based solely on one test trial but, instead, on repeat testing. The best treatment for convergence insufﬁciency is orthoptic convergence exercises.23 The two most useful convergence exercises are near point exercises (pencil pushups) and prism convergence exercises. Near point exercises consist of presenting a target at a remote distance where it is easily fused, then slowly bringing the target in toward the eyes until break point is achieved (Fig. 8-2). With prism convergence exercises, a prism bar oriented base-out is presented to one eye to induce fusional convergence (Fig. 8-3). First, use a small prism that can be easily fused while the patient ﬁxates on a near target. Increase the baseout prism until the patient notes blurred vision (blur point). Then, increase prism until fusion breaks (break point). Both convergence exercises should be repeated 15 to 20 times during each session and repeated 2 to 3 times per day. Convergence exercises stimulate fusional convergence only if the patient appreciates diplopia and the break point. Patients who do not appreciate diplopia can be treated with red glass convergence exercises. A red ﬁlter is placed over the dominant eye and a light is used as the ﬁxation target. The red ﬁlter and light will help the patient recognize diplopia. Convergence exercises have been found to be extremely helpful and curative in patients with convergence insufﬁciency so long as these exercises are diligently performed. Improvement of symptoms usually occurs after a few weeks of exercises, but in some cases several months are needed before symptoms are relieved. In this author’s experience, almost all

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FIGURE 8-2. Near point convergence exercise showing accommodative target at near. Patient starts with the target at arm’s length, and then brings the target toward the nose, converging on the accommodative target.

patients with convergence insufﬁciency can be managed by exercises alone; it is the rare case that requires surgery. Always try orthoptic exercises ﬁrst and, if they fail to alleviate the symptoms, then surgery may be considered. The standard surgery for

FIGURE 8-3. Photograph of child with congenital exotropia.

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convergence insufﬁciency is a small medial rectus resection of one or both medial rectus muscles. In this author’s experience, surgery is not effective in most cases of convergence insufﬁciency.19,35

Accommodative Insufﬁciency A common cause of asthenopia and blurred near vision is convergence insufﬁciency, but occasionally patients have a combination of convergence insufﬁciency and accommodative insufﬁciency.24,35 Even more rare is isolated accommodative insufﬁciency without convergence insufﬁciency.11 Obviously, presbyopia is the most common type of accommodative insufﬁciency, but primary accommodative insufﬁciency can occur in children and young adults as well. Accommodative insufﬁciency can be secondary to a systemic disorder such as Parkinson’s disease, oral lithium, or local ciliary body dysfunction associated with Adie’s pupil.2 According to Duane’s standard curve of accommodation, normal patients under 20 years of age should be able to accommodate at least 10 diopters, or read the 20/40 line on the near card at 10 cm.13 Patients with accommodative insufﬁciency will have a remote near point of accommodation. There are no beneﬁcial exercises for treating accommodative insufﬁciency; however, accommodative exercises can be tried. Mazow et al.23 found modest improvement with pretreatment accommodation averaging 7.1 diopters and posttreatment 11.4 diopters. A reading add can also be prescribed, but prescribe the lowest power that relieves the symptoms and still stimulate some accommodation. Prescribing a strong reading add only weakens the patient’s remaining accommodation.

SENSORY EXOTROPIA If a patient loses vision in one eye, that eye may drift out (sensory exotropia). Patients with dense amblyopia may also develop a sensory exodeviation. It is often said that if the visual loss occurs before 4 years of age, an esotropia develops. If vision loss occurs after 4 years of age, an exodeviation results. This rule, however, is violated as often as it is followed. Studies of patients with unilateral congenital cataracts show an even distribution between esodeviations and exodeviations.10 Treatment

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for sensory exotropia is performing a recession/resection procedure of the eye with the decreased vision.

CONGENITAL EXOTROPIA Congenital exotropia is extremely rare, and most ophthalmologists will see only one or two cases during their career (Fig. 83). Congenital exotropia may occur in patients with systemic disease, craniofacial anomalies, ocular albinism, or cerebral palsy.21 The treatment for congenital exotropia is bilateral lateral rectus recessions, which should be performed after 6 months of age. This syndrome should not be confused with the normal, variable, small-angle exodeviation seen in 70% of normal newborns. Instead, congenital exotropia is a large-angle constant exodeviation, with a relatively poor prognosis for fusion. It has a much higher incidence of amblyopia than intermittent exotropia, with the incidence of amblyopia being similar to congenital esotropia (20 to 40%).

References 1. Archer SM, Sondhi N, Helveston EM. Strabismus in infancy. Ophthalmology 1989;96:133–137. 2. Brown B. The convergence insufﬁciency masquerade. Am Orthopt J. 1990:40:94–97. 3. Burian HLM. Exodeviations: their classiﬁcation, diagnosis and treatment. Am J Ophthalmol 1966;62:1161–1166. 4. Burian HM. The sensorial retinal relationship in comitant strabismus. Arch Ophthalmol 1947;337:336. 5. Burian HM, Franceschetti AT. Evaluation of diagnostic methods for the classiﬁcation of exodeviations. Trans Am Ophthalmol Soc 1970;68:56. 6. Burian HM, Smith DR. Comparative measurement of exodeviations at 20 and 100 feet. Trans Am Ophthalmol Soc 1971;69:188. 7. Burian HM, Spivey BE. The surgical management of exodeviations. Am J Ophthalmol 1965;59:603. 8. Caltrider N, Jampolsky A. Overcorrecting minus lens therapy for treatment of intermittent exotropia. Ophthalmology 1983;90: 1160. 9. Campos EC. Binocularity in comitant strabismus: binocular visual ﬁeld studies. Doc Ophthalmol 1982;53:249. 10. Cheng KP, Hiles DA, Biglan AW, Pettapiece MC. Visual results after early surgical treatment of unilateral congenital cataract. Ophthalmology 1991;98:903–910.

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11. Chrousos GA, O’Neill JF, et al. Accommodative deﬁciency in healthy young adults. J Pediatr Ophthalmol Strabismus 1988;25: 176–179. 12. Costenbader FD. The physiology and management of divergent strabismus. In: Allen JH (ed) Strabismic ophthalmic symposium, vol I. St. Louis: Mosby, 1950:349. 13. Duane A. Studies in monocular and binocular accommodation with their clinical applications. Am J Ophthalmol 1922;5:865–877. 14. Edelman PM, Murphree AL, Brown MH, Wright KW. Consecutive esodeviation . . . then what? Am Orthopt J 1988;38:111–116. 15. Freeman RS, Isenberg SJ. The use of part-time occlusion for early onset unilateral exotropia. J Pediatr Ophthalmol Strabismus 1989;26: 94. 16. Hardesty H. Management of intermittent exotropia. Binoc Vis Q 1990;5:145. 17. Hardesty HH, Boynton JR, Keenan P. Treatment of intermittent exotropia. Arch Ophthalmol 1978;96:268. 18. Henderson JW, Iacobucci I. Occlusion in the pre-operative treatment of exodeviations. Am Orthopt J 1965;15:42. 19. Hermann JS. Surgical therapy for convergence insufﬁciency. J Pediatr Ophthalmol Strabismus 1981;18:28. 20. Hiles DA, Davies GT, Costenbader FD. Long-term observations on unoperated intermittent exotropia. Arch Ophthalmol 1968;80: 436. 21. Hunter DG, Ellis FJ. Prevalence of systemic and ocular disease in infantile exotropia: comparison with infantile esotropia. Ophthalmology 1999;106:1951–1959. 22. Kushner BJ. Exotropic deviations: a functional classiﬁcation and approach to treatment. Am Orthopt J 1988;38:81–93. 23. Mazow ML, Musgrove K, Finkelman S. Acute accommodative and convergence insufﬁciency. Am Orthopt J 1991;41:102–109. 24. Mazow ML. The convergence insufﬁciency syndrome. J Pediatr Ophthalmol Strabismus 1971;8:243–244. 25. Moore S. The prognostic value of lateral gaze measurements in intermittent exotropia. Am Orthopt J 1969;19:69. 26. Nawratzi I, Jampolsky A. A regional hemiretinal difference in amblyopia. Am J Ophthalmol 1958;46:339. 27. Parks MM. Comitant exodeviations in children. In: Strabismus symposium, New Orleans Academy of Ophthalmology. St. Louis: Mosby, 1962:45. 28. Parks MM. Cocomitant exodeviations. In: Ocular motility and strabismus. Hagerstown: Harper & Row, 1975:113–122. 29. Pratt-Johnson JA, Barlow JM, Tillson G. Early surgery in intermittent exotropia. Am J Ophthalmol 1977;84:689. 30. Pratt-Johnson J, Wee HS. Suppression associated with exotropia. Can J Ophthalmol 1969;4:136. 31. Raab EL, Parks MM. Recession of the lateral recti: early and late postoperative alignments. Arch Ophthalmol 1969;82:203.

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32. Richard JM, Parks MM. Intermittent exotropia. Surgical results in different age groups. Ophthalmology 1983;90:172. 33. Scott WE, Keech R, Mash J. The postoperative results and stability of exodeviations. Arch Ophthalmol 1981;99:1814. 34. von Noorden GK, Brown DJ, Parks M. Associated convergence and accommodative insufﬁciency. Doc Ophthalmol 1973;34:393–403. 35. von Noorden GK. Resection of both medial rectus muscles in organic convergence insufﬁciency. Am J Ophthalmol 1976;81:223. 36. von Noorden GK. Some aspects of exotropia. Presented before meeting of the Wilmer Residents’ Association, Johns Hopkins Hospital, April 26, 1966. 37. von Noorden GK. Divergence excess and simulated divergence excess: diagnosis and surgical management. Ophthalmologica 1969;26:719. 38. von Noorden GK. Binocular vision and ocular motility: theory and management of strabismus. St. Louis: Mosby, 1985. 39. Wiggins RE, von Noorden GK. Monocular eye closure in sunlight. J Pediatr Ophthalmol Strabismus 1990;27:16. 40. Wright KW, De Juan E. Patch test with and without 3.00 near add. Wilmer Eye Institute, Johns Hopkins Hospital, 1981 (unpublished data). 41. Wright KW, Min BM, Park C. Comparison of superior oblique tendon expander to superior oblique tenotomy for the management of superior oblique overaction and Brown’s syndrome. J Pediatr Ophthalmol Strabismus 1992;29(2):92–97.

9 Alphabet Patterns and Oblique Muscle Dysfunctions Kenneth W. Wright

I

n this chapter, A- and V-pattern strabismus and oblique dysfunction are discussed, including management strategies. Under the category of A- and V-patterns, special subtypes are described. The section on oblique dysfunction includes the following: head tilt test, inferior oblique paresis and inferior oblique overaction, superior oblique paresis and superior oblique overaction, and Brown’s syndrome.

A- AND V-PATTERNS A signiﬁcant difference in the horizontal deviation from upgaze to downgaze is described as an A- or V-pattern. An A-pattern is described as more divergence in downgaze versus upgaze of at least 10 prism diopters (PD), whereas a V-pattern is increasing divergence in upgaze versus downgaze by 15 PD or more. A- and V-patterns are often a result of oblique muscle overaction or oblique muscle paresis. Other less common causes include nerve misdirection such as Duane’s syndrome, ectopic muscle course with ectopic muscle pulleys, and a rotated orbit associated with craniofacial abnormalities.5,6,29 Examples of strabismus patterns (1 through 5) follow. Example 1. A-pattern ET A-pattern

XT V-pattern

ET V-pattern

XT 10 XT 20 XT 30

ET 30 ET 20 ET 10

XT 30 XT 20 XT 10

ET 10 ET 20 ET 30

Upgaze Primary position Downgaze XT, exotropia; ET, esotropia.

284

V-pattern

XT A-pattern

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A- and V-Pattern Subtypes Look critically at the type of pattern: is it symmetrical or does the change in horizontal deviation occur more in upgaze or downgaze? This is important to know, as the conﬁguration or subtype of the A- or V-pattern can indicate an identifying etiology and can inﬂuence the surgical plan. For example, a V-pattern consisting of convergence in downgaze without signiﬁcant change in horizontal deviation from primary position to upgaze is highly suggestive of a bilateral superior oblique palsy. Listed below are subtypes of A- and V-patterns in which the change in horizontal deviation is asymmetrical.

V-PATTERN SUBTYPES Y-PATTERN The Y-pattern is a V-pattern subtype with divergence occurring in upgaze and little change in the horizontal deviation between primary position and downgaze. This pattern is highly suggestive of bilateral inferior oblique overaction, which is often associated with infantile esotropia and may also be seen with intermittent exotropia. Y-pattern can also be seen in patients with Brown’s syndrome, Duane’s syndrome with upshoot, and rarely congenital aberrant innervation of the lateral rectus muscle with the superior rectus nerve (see Example 2). Example 2. Upgaze Primary position Downgaze

ET Y-pattern

XT Y-pattern

ET 10 ET 25 ET 30

XT 30 XT 15 XT 10

ARROW PATTERN Another V-pattern subtype is convergence that largely occurs between primary position and downgaze. This author has termed this pattern “arrow” pattern. The presence of an arrow pattern and extorsion in downgaze is virtually diagnostic for bilateral superior oblique muscle palsy. The lack of abduction and intorsion in downgaze because of weak superior oblique muscles allows unopposed adduction and extorsion by the inferior recti muscles (see Example 3).

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Example 3. ET Arrow Pattern Upgaze Primary Position Downgaze

Ortho ET 5 ET 20

A-PATTERN SUBTYPE LAMBDA PATTERN The lambda pattern, an A-pattern subtype, is characterized by a divergence in downgaze without much change in the horizontal deviation from primary position to upgaze. A lambda pattern is most frequently associated with bilateral superior oblique overaction. Overrecessed or slipped inferior rectus muscles will also cause an A-pattern lambda subtype with apparent superior oblique muscle overaction. In contrast, inferior oblique muscle underaction causes an A-pattern with most of the horizontal change as convergence in upgaze (see Example 4). Example 4. XT lambda pattern Lambda pattern Upgaze Primary Position Downgaze

XT 15 XT 20 XT 35

X-PATTERN An X-pattern occurs when there is divergence in upgaze and divergence in downgaze, which can occur without a speciﬁc cause. Patients with long-standing large-angle exotropia will frequently show an X-pattern, presumably caused by a tight contracted lateral rectus muscle. As the eye adducts against the tight lateral rectus muscle, it acts as a leash and produces lateral forces. If the eye then rotates up or down the tight lateral rectus slips above or below the eye and pulls the eye up and out, or down and out, respectively. This leash effect of the lateral rectus is also seen in Duane’s syndrome, usually type III, with both an upshoot and downshoot present on attempted adduction. Lateral rectus recessions reduce the X-pattern associated with exotropia, and an ipsilateral lateral rectus recession with a Ysplit works well to reduce the vertical overshoot and X-pattern associated with Duane’s syndrome type III29 (see Example 5).

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Example 5. XT X-Pattern Upgaze Primary position Downgaze

XT40 XT30 XT40

Treatment of A- and V-Patterns A- and V-patterns with minimal or no oblique overaction can be managed by offsetting, or transposing, the horizontal rectus muscles superiorly or inferiorly. Transpose the medial recti insertions toward the apex of the pattern (up for an A-pattern and down for a V-pattern) and the lateral recti insertions to the wide part of the pattern (down for an A-pattern and up for a Vpattern) (Fig. 9-1). An A-pattern exotropia, for example, can be treated by recessing both lateral rectus muscles and transposing them inferiorly (Fig. 9-2). Vertical transposition of horizontal muscles in the treatment of A- or V-patterns changes vector forces and muscle tension as the eyes rotate up and down. For example, when the medial recti are infraplaced for a V-pattern, they gain increased function as the eyes rotate up, thus collapsing the V-pattern. Conversely, when the eyes rotate down, the infraplaced medial rectus muscles slacken, resulting in divergence of the apex of the V-pattern. One-half-tendon-width

FIGURE 9-1. Direction to transpose the rectus muscles to correct for Aand V-patterns. Left diagram: transposition for a V-pattern, with the lateral rectus muscles moved up and medial rectus muscles moved down. Right diagram: transposition for an A-pattern, with the medial rectus muscles moved up and the lateral rectus muscles moved down. The medial rectus is moved toward the apex of the A or V and the lateral rectus is moved away from the apex of the A or V. This transposition holds true whether the muscles are recessed or resected.

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FIGURE 9-2. Drawing of a one-half-tendon-width inferior transposition of the lateral rectus muscle with recession for an A-pattern associated with an intermittent exotropia. A Insertion to limbus distance. B Recession measured from the insertion.

(5 mm) of vertical displacement results in approximately 15 PD of pattern correction. A full-tendon-width vertical displacement results in approximately 25 PD of correction and is reserved for extremely large A- or V-patterns. Vertical transposition of a horizontal rectus muscle by one full-tendon-width reduces the vector forces at the horizontal plane and, in this author’s opinion, often results in unpredictable horizontal alignment. For example, a full-tendon-width infra-placement of the lateral rectus muscles for an A-pattern would predispose to an overcorrection (esotropia) in primary position. This author rarely performs a horizontal rectus muscle transposition more than one-half tendon-width (5 mm) except in cases of a large A- or Vpattern associated with craniofacial disorders or absent muscles. Monocular supraplacement of one rectus muscle and infraplacement of the partner antagonist muscle can be used to correct an A- or V-pattern in a patient with amblyopia to avoid surgery on the only good eye. Monocular A- or V-pattern horizontal muscle offsets can cause signiﬁcant torsional changes and should be done only on amblyopic eyes in patients with poor binocular fusion to avoid inducing torsional diplopia. Thus, monocular horizontal offsets can be used to correct torsional diplopia. In cases with signiﬁcant inferior or superior oblique overaction and an A- or V-pattern, the appropriate oblique muscles should be weakened rather than performing a horizontal rectus muscle transposition. An exception exists for patients with

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superior oblique overaction and binocular fusion. These patients are at risk for developing cyclovertical diplopia after superior oblique tenotomy.23 Patients with binocular fusion and mild superior oblique overaction are best treated with transposition of the horizontal recti rather than a superior oblique tenotomy. Another surgical option for the fusing patient is a controlled tendon elongation procedure, such as the Wright superior oblique tendon expander or a split-tendon elongation. For large A- and V-patterns (25 PD) with 3 or more oblique overaction, consider combining oblique weakening with a half-tendonwidth horizontal rectus muscle transposition.

OBLIQUE DYSFUNCTION Clinical Evaluation of Oblique Dysfunction When an oblique muscle overacts or underacts, all three functions of the muscle are involved: torsional, vertical, and horizontal. Clinical quantiﬁcation of oblique dysfunction, however, is primarily based on the vertical hyper- or hypofunction seen on version testing. To assess oblique function, move the eye under examination into adduction and make an observation. Then move the eye into the ﬁeld of action of the muscle: adduction and elevation for the inferior oblique muscle, and adduction and depression for the superior oblique muscle. The amount of overaction or underaction can be graded on a scale of 1 to 4 for overaction and 1 to 4 for underaction. A measurement of 1 overaction is recorded if there is no hypertropia with horizontal versions, but there is slight overaction when the eye is moved into the ﬁeld of action of the oblique muscle vertically. With 2 overaction, there is a slight hypertropia in horizontal gaze, and with 3 overaction, there is obvious hypertropia on direct horizontal gaze. In 4 overaction, there is a large hypertropia in horizontal gaze with an abduction movement as the eye moves vertically into its ﬁeld of action. Figure 5-3 in Chapter 5 shows degrees of inferior oblique overaction on version testing. The amount of A- or V-pattern and amount of fundus torsion are additional parameters to help quantitate the amount of oblique dysfunction. When evaluating oblique dysfunction, the abducting eye should be ﬁxing so the adducting eye is free to manifest oblique dysfunction. For example, when the right inferior oblique is

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being evaluated, a version movement to the left is directed, the right eye is partially covered, and the right eye is observed behind the cover for an upshoot (see Chapter 5, Fig. 5-4). Discussion of the characteristics of individual oblique muscle dysfunctions follows.

Primary Oblique Overaction Versus Paresis Overaction of an oblique muscle can be primary (i.e., unknown etiology) or can be secondary to a muscle paresis. Primary oblique muscle overaction is commonly found in association with A- and V-pattern horizontal strabismus. One possible etiology for what appears to be primary oblique muscle overaction is ectopic location of rectus muscles and their pulleys.5,6 A transient congenital oblique muscle paresis could also cause secondary overaction of its antagonist muscle. A congenital superior oblique paresis, for example, produces ipsilateral inferior oblique overaction. Oblique overaction can also be caused by paresis of its yoke vertical rectus muscle of the contralateral eye (Hering’s law of yoke muscles). For example, a left inferior rectus paresis causes apparent overaction of the right superior oblique muscle and is best observed when the patient ﬁxes with the paretic left eye, down and in abduction. In general, acquired oblique muscle paresis is associated with underaction of the agonist and with relatively mild overaction of the antagonist oblique muscle. Congenital and longstanding oblique muscle paresis are usually associated with minimal superior oblique underaction and signiﬁcant overaction of the antagonist oblique muscle. The head tilt test, described below, is used to distinguish primary oblique dysfunction from oblique dysfunction secondary to a vertical or oblique muscle paresis. A positive head tilt test is a strong indication that there is a vertical rectus or oblique muscle paresis whereas a negative head tilt usually indicates a primary oblique overaction. If the vertical deviation changes by more than 5 PD on right tilt versus left tilt, then the head tilt test is said to be positive. If there is no signiﬁcant difference in the deviation (5 PD or less) from right tilt to left tilt, then the head tilt test is said to be negative.

BIELSCHOWSKY HEAD TILT TEST Tilting the head stimulates the utricular reﬂex and invokes torsional eye movements to correct and maintain the appropriate

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retinal orientation. A tilt right, for example, invokes intorsion of the right eye and extorsion of the left eye. The intortors are the superior oblique and the superior rectus muscles, and the extortors are the inferior oblique and the inferior rectus muscles. This arrangement keeps vertical forces balanced during the head tilt. If one of the torsional muscles is paretic, then there will be an imbalance of vertical forces and a vertical deviation will occur on head tilt testing. Figure 9-3 demonstrates this concept for a right superior oblique paresis. As the head tilts to the right, the right superior oblique and right superior rectus contract to intort the right eye. Because the superior oblique is paretic, the superior rectus has unopposed vertical force and elevates the eye, creating an increasing right hyperdeviation on head tilt to the right. The head tilt test is used in patients with a vertical deviation to determine if either a vertical rectus or oblique muscle is paretic. When a patient presents with a vertical deviation, ﬁrst perform the head tilt test to see if a paretic muscle is present. If the head tilt test is positive (5 PD difference in right tilt vs. left tilt), then it is likely there is a vertical rectus or oblique muscle paresis. To determine which muscle is paretic, measure the deviation in sidegaze and use the three-step test as described next.

FIGURE 9-3. Diagram of a right superior oblique paresis with a positive head tilt in tilt right. As the head tilts to the right, the left eye extorts and the right eye intorts. The extorters of the left eye are the inferior rectus and the inferior oblique. Their vertical functions cancel each other, so there is no vertical overshoot. The intortors of the right eye are the superior rectus (SR) and superior oblique (SO) muscles. Because the right superior oblique is paretic, the elevation effect of the superior rectus is unopposed, and a right hypertropia occurs on tilt to the right.

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PARKS THREE-STEP TEST Marshall Parks in 1958 published the “Three-Step Test” for the diagnosis of cyclovertical muscle palsies.23 This test identiﬁes which muscle is paretic in patients with a hypertropia caused by an isolated vertical rectus muscle or oblique muscle palsy. The three steps are to determine (1) which paretic muscle might be causing the hyperdeviation in primary position, (2) where the hypertropia is greatest, in rightgaze or leftgaze, and (3) on head tilt, which side the hypertropia is greatest: tilt right or tilt left. See Table 9-1 for results of the three-step test for both vertical and oblique muscle palsy. The ﬁrst step is to determine which paretic muscle could be causing a hyperdeviation in primary position. A right hyperdeviation, for example, might be caused by a weak depressor muscle of the right eye (i.e., right inferior rectus or right superior oblique) or a weak elevator muscle of the left eye (i.e., left superior rectus or left inferior oblique). The second step is to determine in which horizontal ﬁeld of gaze the hypertropia increases. If the hypertropia increases on gaze away from the hypertropic eye, the paretic muscle is the

TABLE 9-1. Responses to the Three-Step Test for All Vertical and Oblique Muscle Palsies.

First step: hyper in primary

Second step: hyper increases in gaze

Third step: hyper increases with head tilt (hyper ⬎ ipsilateral tilt ⫽ oblique hyper ⬎ contralateral tilt ⫽ vertical rectus)

RIR

R LIO

LIO

L RIR

RSO

R RSO

LSR

L LSR

RSR

R RSR

LSO

L LSO

RIO

R LIR

LIR

L RIO

RSO RIR RHT vs.

R LSR LIO L RSR RIO

LHT vs.

R LSO LIR L

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ipsilateral oblique or contralateral vertical rectus. A hypertropia that increases to the side of the hypertropia is caused by a paretic vertical muscle on the side of the hypertropia or the contralateral vertical rectus muscle, that is, the paretic muscle is a vertical rectus muscle of the abducting eye or an oblique muscle of the adducting eye. For example, a right hyperdeviation that increases in leftgaze could only be caused by a paretic left superior rectus muscle or a paretic right superior oblique muscle. The third step is based on the Bielschowsky head tilt test as previously described. This last step can be difﬁcult to calculate, so this author uses a trick that he shamelessly calls Wright’s rule. The author states, “I am sure others have used the same trick to simplify the head tilt test, but I like the way it sounds: Wright’s Rule.” Wright’s rule states that if the hyperdeviation increases on head tilt to the same side of the hyperdeviation, then an oblique muscle is paretic. If the hyperdeviation increases to the opposite side of the hyperdeviation, then a vertical rectus muscle is paretic. For example, if the right hyper increases on head tilt to the right (same side as the hyper), then the oblique muscle is paretic; namely, the right superior oblique (SO) or left inferior oblique (IO) muscle. If the right hyper increases on left head tilt (opposite side of the hyper), then it is the vertical rectus muscle that is weak; namely, the left superior rectus (SR) muscle or right inferior rectus (IR) muscle. Example 6 describes characteristics of a right superior oblique paresis. Example 6. Right Superior Oblique Paresis Rightgaze RHT10

Leftgaze RHT 15

RHT 25

Head tilt test: right, RHT 15 PD; left, RHT 4 PD.

PARKS THREE-STEP TEST

FOR

EXAMPLE 6

Step 1: Right hypertropia Right IR or SO versus left SR or IO (underacting muscles, right eye vs. left eye). Step 2: Right hypertropia increases in leftgaze Left SR or right SO (the muscles with ﬁeld of action in leftgaze). Step 3: Right hypertropia increases in head tilt to the right Right tilt induces intorsion of the right eye and extorsion of left eye. Both the muscles in contention (RSO and LSR) are

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intortors, but only the RSO intorts on right tilt. Therefore, the diagnosis is right superior oblique paresis. or, by Wright’s rule: Right hyperdeviation increases on right head tilt (same side as the hyper); therefore, it has to be an oblique muscle paresis. As we are down to two choices from step 2, RSO and LSR, the paretic muscle is the right superior oblique.

SHORTCUT

TO THE

THREE-STEP TEST

Classically, the paretic muscle is determined by the Parks threestep test as just described. In 1967, Helveston13 described combining steps 1 and 2 to make a two-step test. This author prefers to start with the head tilt test and use Wright’s rule. To know which vertical rectus or oblique muscle is weak, determine in which horizontal gaze the vertical deviation increases, right or left. As an example, a right hypertropia that increases on head tilt to the right and increases on rightgaze has to be caused by an oblique muscle paresis because the tilt is positive to the same side as the hypertropia. Because the right hypertropia increases on rightgaze, in the ﬁeld of action of the left inferior oblique muscle (not in the ﬁeld of action of the right superior oblique muscle), the paretic muscle is the left inferior oblique. Using Wright’s rule alone narrows the choices to two muscles: either an oblique or a vertical rectus muscle of each eye. Determining the horizontal gaze where the hypertropia is greatest tells us which eye, the right eye or the left eye.

PROBLEMS

WITH THE

HEAD TILT TEST

A positive head tilt test is not infallible when diagnosing cyclovertical muscle paresis. Patients with dissociated vertical deviations, as well as some patients with intermittent exotropia, show a positive head tilt. In addition, the head tilt test is designed to diagnose an isolated paretic muscle, and it may not be reliable when multiple muscles are paretic or if an ocular restriction is present.

Superior Oblique Paresis A superior oblique paresis is the most common cause for an isolated vertical deviation. The typical ﬁndings of a unilateral superior oblique paresis include an ipsilateral hypertropia that increases on contralateral side-gaze and a positive head tilt test with the hyperdeviation increasing on head tilt to the ipsilateral

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shoulder (see Example 6). There may be relatively little superior oblique underaction and mostly inferior oblique overaction (Fig. 9-4A,B). Mild extorsion is recorded if less than 10°. To reduce the hypertropia and fuse, patients with a unilateral superior oblique paresis adopt a compensatory head tilt to the side, opposite the paresis, combined with a face turn away from the side of the palsy. Long-standing unilateral superior oblique paresis with a large hypertropia may show pseudosuperior oblique overaction of the contralateral eye, as a result of contraction of the ipsilateral superior rectus muscle because of the long-standing hypertropia and Hering’s Law of yoke muscles. As the ipsilateral eye has restricted depression in abduction, the yoke muscle overacts (i.e., contralateral superior rectus muscle).

FIGURE 9-4A,B. Composite nine-gaze photograph of patient with a congenital right superior oblique palsy. Note the large RHT in primary position that increases in leftgaze. There is 3 right inferior oblique overaction and 2 superior oblique underaction. In straight rightgaze, it appears that the left superior oblique is overacting, but the right superior oblique is slightly tight because of secondary contracture. (B) Positive head tilt test with large RHT on tilt right.

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FIGURE 9-5. Composite nine-gaze photograph of patient with bilateral traumatic superior oblique palsy. Patient has a small esotropia and extorsion in primary position that increases in downgaze. Note the V-pattern (arrow pattern subtype) with a large esotropia in downgaze. There is also severe underaction of both superior oblique muscles associated with relatively mild inferior oblique overaction.

Bilateral superior oblique paresis is associated with bilateral superior oblique underaction, a V-pattern (arrow subtype), little or no hypertropia, and a right hypertropia in leftgaze and a left hypertropia in rightgaze (Fig. 9-5). Other signs include a bilateral extorsion (total greater than 10°), a reversing head tilt test with a right hypertropia in tilt right, and a left hypertropia in tilt left. The presence of an arrow pattern with extorsion increasing in downgaze (Example 7) is diagnostic for an acute bilateral superior oblique palsy and is often seen with traumatic superior oblique palsies. Clinical signs of unilateral versus bilateral superior oblique paresis are shown in Table 9-2. Example 7. Bilateral Superior Oblique Paresis Rightgaze LHT10

Leftgaze RHT 2, ET4 RHT 5, ET 20

Bilateral Maddox Rod—15° Extorsion. Bilateral extorsion on fundus exam. Head tilt test: right, RHT 10 PD; left, LHT 10 PD. ET on downgaze

RHT 10

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TABLE 9-2. Unilateral Versus Bilateral Superior Oblique Paresis. Clinical sign

Unilateral

Bilateral

Superior oblique underaction Inferior oblique overaction V-pattern

Ipsilateral underaction Ipsilateral overaction Less than 10 PD

Hypertropia

Greater than 5 PD

Head tilt test

Increasing hyper on ipsilateral head tilt (Rt SOP RH tilt right) Less than 10°

Bilateral underaction Bilateral overaction Greater than 10 PD with arrow pattern (convergence in downgaze) Less than 5 PD (except asymmetrical paresis) Positive head tilt to both sides (RHT on right tilt and LHT on left tilt)

Extorsion

Greater than 10°

A bilateral asymmetrical superior oblique paresis can look like a unilateral superior oblique paresis; this is termed masked bilateral superior oblique paresis.16,17 Suspect a masked bilateral paresis if the hypertropia precipitously diminishes in lateral gaze toward the side of the obvious paretic superior oblique muscle and if there is even slight inferior oblique overaction of the fellow eye (see Example 8). Example 8. Masked Bilateral Superior Oblique Paresis Rightgaze RHT5

Leftgaze RHT 20

RHT 30

Head tilt test: right, RHT 25 PD; left, RHT 3 PD.

The presence of a V-pattern and bilateral extorsion on fundus examination also suggest bilateral involvement in patients with a presumed unilateral paresis. In these cases of masked bilateral superior oblique paresis, if surgery is performed only for a unilateral superior oblique palsy, the contralateral superior oblique paresis will become evident postoperatively.

FALLEN EYE Signiﬁcant underaction of the superior oblique muscle and ﬁxation with the paretic eye will produce the classic ﬁnding called the fallen eye. When a patient with a superior oblique paresis ﬁxes with the paretic eye and tries to look into the ﬁeld of action of the paretic superior oblique muscle, the weak superior oblique muscle requires a large amount of innervation to make the eye

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FIGURE 9-6. Photograph of a traumatic right superior oblique palsy, showing the fallen eye, left eye. The right eye is ﬁxing in the ﬁeld of action of its paretic superior oblique muscle (i.e., down and in adduction), requiring a great deal of innervation. Because of Hering’s law of equal innervation of yoke muscles, the left inferior rectus muscle (yoke muscle to the paretic right superior oblique muscle) also receives a great deal of innervation. Because the left inferior rectus is at full strength, it overacts and pulls the left eye down, thus causing the appearance of a left fallen eye.

move down and nasally. Because of Hering’s law, the yoke muscle (contralateral inferior rectus muscle) receives an equally large amount of innervation. Because the contralateral inferior rectus muscle has normal function, this increased innervation produces a large secondary hypotropia, or the fallen eye (Fig. 9-6).

INHIBITIONAL PALSY ANTAGONIST

OF THE

CONTRALATERAL

Chavasse, in 1939, described the term inhibitional palsy of the contralateral antagonist. This term relates to a patient who chronically ﬁxates with the paretic eye, resulting in an apparent weakness on version testing of the yoke muscle to the antagonist of the paretic eye. That is, the paretic eye moves easily into the ﬁeld of its antagonist with little innervation because the agonist is weak. The yoke muscle to the antagonist of the paretic muscle receives the same small innervation (Hering’s law), so it

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will appear paretic on versions because its antagonist is innervated. Clinically, this is seen in association with a congenital fourth nerve palsy and ipsilateral inferior oblique overaction when the patient ﬁxates with the paretic eye. For example, a left fourth nerve palsy with left inferior oblique overaction will produce a left hypertropia increasing in rightgaze. If the patient ﬁxates with the left eye, the innervation required for the left eye to look up and right is minimal, as it is in the ﬁeld of the overacting left inferior oblique muscle. The yoke muscle to the left inferior oblique muscle is the right superior rectus muscle, and it too will receive little innervation. The right superior rectus will appear to underact or be paretic because its antagonist, the right inferior rectus, is normally innervated and holds the eye down. Inhibitional palsy of the contralateral antagonist is only seen on version testing when the paretic eye is ﬁxing.

PRIMARY INFERIOR OBLIQUE OVERACTION VERSUS SUPERIOR OBLIQUE PALSY Primary inferior oblique overaction can be differentiated from superior oblique palsy by the head tilt test and type of V-pattern (Table 9-3).

Traumatic Superior Oblique Paresis Traumatic superior oblique paresis is usually associated with severe closed head trauma, loss of consciousness, and cerebral concussion; however, even very mild head trauma without loss of consciousness can cause a superior oblique paresis. Traumatic superior oblique paresis occurs when the tentorium traumatizes

TABLE 9-3. Primary Inferior Oblique Overaction Versus Superior Oblique Paresis. Clinical sign

Primary overaction

Superior oblique paresis

Inferior oblique overaction V-pattern Head tilt test Subjective torsion

Yes Yes, Y-pattern Negative No

Objective extorsion (fundus examination) Underaction of ipsilateral superior oblique muscle

Yes

Yes Yes, “arrow” pattern Positive Yes (except in congenital superior oblique paresis) Yes

No (minimal if any)

Yes

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the trochlear nerves as they exit the posterior midbrain posteriorly. Since the two trochlear nerves exit the midbrain together, only a few millimeters apart, the nerve trauma is almost always bilateral. Thus, most cases of traumatic superior oblique paresis are bilateral, although the paresis may be asymmetrical. The pattern of strabismus is classically, minimal or no hypertropia in primary position, a left hypertropia in rightgaze, a right hypertropia in leftgaze, underaction of both superior oblique muscles, and an esotropia in downgaze (Figs. 9-5, 9-6). There is a positive head tilt with a right hypertropia on right tilt and a left hypertropia on left tilt. Extorsion increasing in downgaze can be demonstrated by Maddox rod and indirect ophthalmoscopy. Patients complain of horizontal or vertical torsional diplopia that is worse in downgaze (Fig. 9-5). In most cases, there is not much ipsilateral inferior oblique muscle overaction, usually 1 or less. Because the strabismus is acquired, patients complain of diplopia—torsional, vertical, and horizontal—that increases in downgaze. The management of traumatic superior oblique paresis is discussed later in this chapter under Treatment of Superior Oblique Paresis.

Congenital Superior Oblique Paresis The cause of congenital superior oblique paresis is usually unknown. The paresis may be associated with a lax superior oblique tendon or rarely an absent tendon.12 Most cases present as a unilateral paresis or an asymmetrical masked bilateral paresis. Typically, there is a large hypertropia in primary position and signiﬁcant inferior oblique overaction, usually with relatively little superior oblique underaction (see Fig. 9-4). The most common presenting sign is a head tilt opposite to the side of the palsy. Even though the paresis is present at birth, symptoms often occur in late childhood or even adulthood. It is common for patients to be diagnosed for the ﬁrst time in middle age. Normally vertical fusional amplitudes are weak and even small acquired hyperdeviations of 3 to 5 PD cannot be fused and result in constant diplopia. Patients with congenital superior oblique paresis, however, develop large vertical fusional amplitudes, and fuse large hypertropias up to 35 PD. The presence of large vertical fusion amplitudes is an important clinical sign that the hyperdeviation is long-standing, rather than acutely acquired, and is suggestive of a congenital superior oblique palsy.

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Over time, the fusional control weakens, resulting in a deviation that becomes manifest in later life. In addition to large fusional vergence amplitudes, patients with congenital superior oblique paresis adopt a compensatory head tilt opposite to the palsy to minimize the deviation and establish binocular fusion. Patients with congenital superior oblique paresis typically have good stereopsis and manifest the hyperdeviation intermittently, usually when fatigued. Even though patients with congenital superior oblique paresis have high-grade stereopsis, most also have the ability to suppress when tropic so that they usually do not experience diplopia. This sensory adaptation is similar to the adaptation of patients with intermittent exotropia. Typically these patients also do not demonstrate extorsion by Maddox rod testing as they adapt to the retinal extorsion. Facial asymmetry is seen in approximately 75% of patients with congenital superior oblique palsy, with one side of the face being hypoplastic and smaller.26 The hypoplastic side of the face is on the side of the head tilt (i.e., the dependent side of the face) (Fig. 9-7). One theory for the facial asymmetry is that gravita-

FIGURE 9-7. Photograph of patient with a compensatory right head tilt and right face turn associated with a left congenital superior oblique palsy. Note the facial asymmetry, as the right side of the face is hypoplastic. Hypoplasia is ipsilateral to the head tilt and contralateral to the superior oblique palsy.

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tional pull on the dependent side of the face causes changes in size of facial structures. Another theory is that facial asymmetry represents a mild form of congenital plagiocephaly associated with the superior oblique palsy. In summary, signs that a superior oblique palsy is congenital and not acquired include childhood photographs showing a long-standing head tilt, facial asymmetry, lack of extorsional diplopia, lack of extorsion by Maddox rod, and large vertical fusion amplitudes. In most cases, the diagnosis of congenital superior oblique muscle palsy can be made on the basis of clinical evaluation.

Other Causes of Superior Oblique Paresis The majority of superior oblique pareses are either congenital or traumatic, but other causes include vascular disease with brainstem lacunar infarcts, multiple sclerosis, intracranial neoplasm, herpes zoster ophthalmicus, diabetes and associated mononeuropathy, and iatrogenic after superior oblique tenotomy. An acquired idiopathic superior oblique paresis requires a neurological workup including neuroimaging. Patients with craniosynostosis may have bilateral superior oblique palsies caused by absent superior oblique tendons.

Treatment of Superior Oblique Paresis The treatment of superior oblique paresis depends on the pattern of the strabismus. Cardinal position of gaze measurements and evaluation for inferior oblique overaction and superior oblique underaction are needed to determine the pattern of strabismus and where the deviation is greatest. Subjective torsion should be assessed by double Maddox rod testing in acquired cases; however, patients with a congenital superior oblique palsy will not have subjective torsion. Objective torsion evaluated by indirect ophthalmoscopy can be useful for verifying torsional abnormalities but is usually not the major clinical sign that directs the treatment plan. Most treatment strategies require identifying where the hypertropia is greatest, and surgery is then designed to correct the deviation in primary position while reducing the incomitance.15 For example, a right unilateral superior oblique paresis with a hypertropia less than 10 PD in primary position, inferior oblique overaction, and minimal superior oblique underaction

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can be treated with a simple ipsilateral inferior oblique weakening procedure (e.g., inferior oblique muscle graded anteriorization). If the hypertropia in primary position is greater than 15 PD, then an isolated inferior oblique recession may not be enough to correct the hypertropia. In this case, especially if there is a signiﬁcant hypertropia in downgaze, one should add a contralateral inferior rectus recession to an ipsilateral inferior oblique recession (Table 9-4). Late overcorrections have been known to occur after inferior rectus recessions. This author has changed to a nonabsorbable suture or a long lasting absorbable suture for inferior rectus muscle recessions, and this choice seems to have solved the late overcorrection problem. In cases of congenital superior oblique palsies, be conservative in regard to recessing the contralateral inferior rectus muscle. A small undercorrection is usually well tolerated, but an overcorrection and a reverse hypertropia is difﬁcult for these patients to fuse. Tightening the entire width of the superior oblique tendon by performing a superior oblique tuck has theoretical utility for improving superior oblique function. A superior oblique tuck, however, usually results in minimal to no improvement of superior oblique function, and the tight tendon creates a restrictive leash of elevation in adduction (i.e., iatrogenic Brown’s syndrome). The tuck has been suggested for patients with congenital superior oblique paresis secondary to a lax superior oblique tendon.12,27 Plager27 suggests performing exaggerated forced duction testing of the superior oblique tendon at the beginning of surgery to see if the tendon is lax or absent. Caution should

TABLE 9-4. Treatment of Unilateral Superior Oblique Paresis. Clinical manifestation

Procedure

Inferior oblique overaction: small hypertropia Hyperdeviation in primary position 15 PD; deviation is greater in upgaze Inferior oblique overaction: large hypertropia Hyperdeviation in primary position 15 PD Lax superior oblique tendon with superior oblique underaction Hyperdeviation in primary position 15 PD; minimal inferior oblique overaction; deviation is greatest in downgaze

Inferior oblique weakening (author prefers graded anteriorization) (common) Ipsilateral inferior oblique weakening (author prefers graded anteriorization), with contralateral inferior rectus recession (common) Small superior oblique tuck (rare)

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be used when tucking the superior oblique, as iatrogenic Brown’s syndrome is a frequent complication of a superior oblique tendon tuck. Most surgeons avoid the superior oblique tuck unless there is signiﬁcant superior oblique underaction and an extremely lax tendon or, in cases of bilateral superior oblique paresis, where there is severe superior oblique underaction. Traumatic superior oblique palsies should be observed for 6 months following recovery of muscle function. Patients who have partial recovery of superior oblique muscle function will often be left with extorsional diplopia worse in downgaze, without signiﬁcant oblique dysfunction, V-pattern, or hypertropia. In these cases, extorsion can be improved by the Harada–Ito procedure, which consists of selectively tightening the anterior one-fourth to one-third of the superior oblique tendon ﬁbers.11 Patients with a bilateral superior oblique palsy and poor recovery of muscle function show a large esotropia in downgaze (arrow subtype V-pattern), extorsion greater in downgaze, left hypertropia in rightgaze, and a right hypertropia in leftgaze, but minimal or no hypertropia in primary position. In these cases, consider either bilateral Harada–Ito procedures and bilateral medial rectus muscle recessions with infraplacement one-half-tendon-width or bilateral superior oblique tendon tucks and bilateral medial rectus muscle recessions with infraplacement one-half-tendon-width. This is a difﬁcult strabismus to correct; however, surgery can often improve diplopic symptoms. The superior oblique tucks will create a bilateral iatrogenic Brown’s syndrome, but this may be an acceptable trade-off for improved single binocular vision in downgaze. Table 9-4 lists treatment strategies for unilateral superior oblique paresis, and Table 9-5 lists treatments for bilateral superior oblique paresis.

Inferior Oblique Paresis An isolated inferior oblique paresis is extremely rare and, when it does occur, it is usually idiopathic. Pollard28 reported on 25 patients having an isolated inferior oblique palsy, with 23 being unilateral and 2 bilateral. All cases were idiopathic and benign without an identiﬁable neurological cause. Rarely, inferior oblique palsy has been reported after head trauma20 or attributed to a microvascular occlusive event. Patients with isolated inferior oblique paresis show ipsilateral superior oblique overaction, but they can be distinguished from those with primary superior

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TABLE 9-5. Treatment of Bilateral Superior Oblique Paresis. Clinical manifestation

Procedure

Extorsional diplopia (partially recovered traumatic SOP) Extorsional diplopia (5°), minimal hypertropia, 8 PD, small or no V-pattern (10 PD), and minimal inferior oblique overaction and superior oblique underaction

Bilateral Harada–Ito

Bilateral superior oblique underaction or (often traumatic SOP, rarely congenital lax SO tendon)

Bilateral superior oblique tendon tuck with bilateral medial rectus recessions with inferior transposition one-half tendon width

Hypertropia 8 PD and big arrow pattern (15 PD increase in esotropia from primary to downgaze), 10° extorsion in primary position increasing in downgaze, and reversing hypertropias in sidegaze Masked bilateral or asymmetrical bilateral superior oblique palsy (usually congenital SOP)

Hyperdeviation in primary position 10 PD, asymmetrical inferior oblique overaction

Bilateral inferior oblique graded anteriorization (more anteriorized on the side of the obvious SOP) and recession of inferior rectus contralateral to the obvious SOP or If associated with a large head tilt, bilateral inferior oblique graded anteriorization (more anteriorized on the side of the obvious SOP) and Harada–Ito on the side of the obvious SOP

oblique overaction. Unlike primary superior oblique overaction, inferior oblique paresis is associated with a positive head tilt test and a hyperdeviation that is greatest when the patient looks up and in a horizontal gaze away from the affected eye. For example, a left inferior oblique paresis results in a right hypertropia that increases in rightgaze and upgaze, and the hyperdeviation increases on head tilt to the right. Note that, on versions, inferior oblique paresis looks similar to Brown’s syndrome with limited elevation in adduction; however, there is an A-pattern and superior oblique overaction with an inferior oblique palsy, and forced ductions are negative (Table 9-6). The treatment of a unilateral inferior oblique paresis is an ipsilateral superior oblique weakening procedure (e.g., Wright

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TABLE 9-6. Differential Diagnoses of Elevation Deﬁcit in Adduction.

Bilateral involvement Pattern Superior oblique overaction Inferior oblique underaction Standard forced ductions Head tilt test Torsion

Greatest vertical deviation

Brown’s syndrome

Primary superior oblique overaction

Inferior oblique paresis

Unusual

Common

Unusual

“Y” (divergence in upgaze) No

Lambda (divergence in downgaze) Yes

“A” (convergence in upgaze) Yes

Yes

Minimal to moderate Negative

Yes

Positive Negative None to slight intorsion in upgaze Upgaze

Negative Intorsion (increasing in downgaze) Downgaze

Negative Positive Intorsion (increasing in upgaze) Upgaze

superior oblique tendon expander) if the hypotropia is less than 10 PD, or add a recession of the contralateral superior rectus recession if the hypotropia is greater than 10 PD.30

Superior Oblique Overaction The cause of superior oblique overaction (SOOA) is unknown. It may be related to an associated paresis of the contralateral inferior rectus muscle, thus producing a secondary overaction of the yoke superior oblique muscle. The author has noted several patients with superior oblique overaction who also have an underacting contralateral inferior rectus muscle.

CLINICAL FEATURES OF SUPERIOR OBLIQUE OVERACTION Superior oblique overaction is an exaggeration of the normal function of the superior oblique muscle that includes intorsion, depression, and abduction. Patients with superior oblique overaction show a downshoot of the adducting eye in lateral gaze, abduction in downgaze causing an A-pattern, and intorsion that is seen on indirect ophthalmoscopy. The A-pattern is not symmetrical, but shows more divergence from primary position to downgaze than from upgaze to primary position. This type of Apattern is termed a lambda pattern (Fig. 9-8).

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Superior oblique overaction often occurs in association with horizontal strabismus such as intermittent exotropia. Most patients with superior oblique overaction do not show subjective incyclotorsion with Maddox rod testing, even though indirect ophthalmoscopy reveals intorsion, because sensory adaptation of the superior oblique overaction has been present since early infancy. Like inferior oblique overaction, superior oblique overaction is usually bilateral. Another characteristic of superior oblique overaction is limited elevation in adduction, which is secondary to a contracted tight superior oblique muscle.

DIFFERENTIAL DIAGNOSIS OF SUPERIOR OBLIQUE OVERACTION The differential diagnosis of limited elevation in adduction includes superior oblique overaction, Brown’s syndrome, and inferior oblique paresis (Table 9-6). Brown’s syndrome is caused by a tight superior oblique muscle–tendon complex. In Brown’s syndrome, there is no superior oblique overaction, and forced ductions are positive to elevation in adduction. In addition, the syndrome is often associated with an exodeviation when the eyes move from primary position to upgaze (Y-pattern), whereas superior oblique overaction is associated with a lambda Apattern.

FIGURE 9-8. Composite nine-gaze photograph of a patient with intermittent exotropia and bilateral superior oblique overaction (3 OU) with typical A-pattern (lambda subtype) with increasing divergence in downgaze.

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TREATMENT OF SUPERIOR OBLIQUE OVERACTION The ideal superior oblique weakening procedure produces a measured slackening of the muscle–tendon complex without disrupting the functional mechanics of the insertion. Many surgical approaches to weaken the superior oblique have been tried.3,31 Presently, the two procedures most commonly used are the superior oblique tenotomy and the Wright silicone tendon expander.38,41 The tenotomy technique involves cutting the tendon in two, while the silicone tendon expander consists of inserting a segment of a 240 retinal silicone band (4–6 mm) between the cut ends of a nasal tenotomy to elongate the tendon.42 Other superior oblique weakening procedures include tenectomy, recession, and posterior tenotomy.3,31 In a comparative study, this author found the silicone tendon expander procedure to be superior to a tenotomy, especially in patients with preoperative fusion.40 Performing a superior oblique tenotomy on patients with high-grade stereopsis and fusion carries a signiﬁcant risk for creating a secondary superior oblique paresis and causing postoperative diplopia.25 In these cases, the silicone tendon expander is preferred. Another situation where superior oblique weakening procedures can cause problems is in patients with preexisting dissociated vertical deviation (DVD); weakening the superior obliques will exacerbate DVD. In these cases, options are to treat the A-pattern with horizontal rectus muscle transpositions rather than weakening the superior obliques, or to plan an undercorrection of the superior oblique overaction with the silicone tendon expander. The advantage of the superior oblique silicone tendon expander is that it lengthens the superior oblique tendon in a controlled manner and holds the cut tendon ends apart at a ﬁxed distance. This technique reduces postoperative superior oblique paresis, allows for controlled weakening, and makes it possible to ﬁnd cut tendon ends if a reoperation is necessary.

Inferior Oblique Overaction Primary inferior oblique overaction is most commonly associated with a horizontal strabismus such as congenital esotropia or intermittent exotropia. Isolated primary inferior oblique overaction can also occur without associated horizontal strabismus. Although primary inferior oblique overaction is bilateral, in

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most cases it can be quite asymmetrical, with the lesser overacting inferior oblique muscle difﬁcult to detect.24 When inferior oblique overaction is identiﬁed, it is important to differentiate primary inferior oblique overaction from a secondary inferior oblique overaction (i.e., superior oblique paresis). It can be difﬁcult to differentiate primary inferior oblique overaction from secondary overaction, as patients with marked inferior oblique overaction may have signiﬁcant superior oblique underaction secondary to the tight inferior oblique muscle. On the other hand, patients with a superior oblique paresis often have inferior oblique overaction. In addition, indirect ophthalmoscopy will show signiﬁcant objective extorsion in both primary and secondary inferior oblique overaction. The key to distinguishing primary from secondary inferior oblique overaction is the head tilt test. The head tilt test is negative in primary inferior oblique overaction and is positive with secondary inferior oblique overaction. In both groups, there is the typical upshoot of the adducting eye, and both types usually manifest a signiﬁcant V-pattern, especially if there is bilateral inferior oblique overaction. The type of V-pattern, however, can help differentiate primary versus secondary inferior oblique overaction. Patients with primary inferior oblique overaction have a Y-pattern with a signiﬁcant exotropia shift occurring from primary position to upgaze but relatively little change between primary position and downgaze (Fig. 9-9). The Y-pattern

FIGURE 9-9. Composite nine-gaze photograph of patient with bilateral primary inferior oblique overaction. There is a large V-pattern (Y-subtype) with divergence in upgaze. The inferior oblique overaction is 3 OU with no signiﬁcant superior oblique underaction.

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occurs because the inferior oblique muscles act as abductors in upgaze. In contradistinction, a V-pattern associated with superior oblique paresis (especially bilateral) shows an arrow pattern with an esotropic shift that occurs when moving from primary position to downgaze. Because the inferior oblique muscle is an extortor, elevator, and abductor, these elements are exaggerated in direct proportion to the overaction. When quantitating inferior oblique overaction, look at the entire function of the muscle, including the upshoot, amount of V-pattern, and fundus extorsion.10,37 See Table 9-3 for a comparison of the clinical signs of primary inferior oblique overaction with secondary inferior oblique overaction caused by superior oblique paresis.

MIMICKERS OF INFERIOR OBLIQUE OVERACTION Inferior oblique overaction is the most common cause of an ocular upshoot in adduction. Dissociated vertical deviation (DVD) can look just like inferior oblique overaction, because DVD will become manifest in sidegaze as the adducted eye is occluded by the nasal bridge (see Chapter 10); this results in a hyperdeviation in sidegaze that mimics inferior oblique overaction. DVD can be differentiated from inferior oblique overaction by occluding the affected eye in abduction as well as adduction and evaluating for a change in the vertical deviation. If the elevation is the same in adduction and abduction, then this is DVD, whereas an increasing hyperdeviation in adduction suggests inferior oblique overaction. Because DVD commonly coexists with inferior oblique overaction in patients with infantile esotropia, the distinction can be extremely difﬁcult to see. Distinguishing clinical features such as the presence of a Vpattern (Y-subtype), a true hyperdeviation in lateral gaze with a hypotropia of the contralateral eye, and objective extorsion on indirect ophthalmoscopy will help to identify inferior oblique overaction rather than DVD. An upshoot in adduction can be caused by a tight lateral rectus muscle. As the eye adducts and slightly elevates, the tight lateral rectus pulls the eye up, causing pseudo-overaction of the inferior oblique. Aberrant innervation of the inferior oblique and superior rectus muscles has been documented as causing an upshoot associated with Duane’s syndrome (see Chapter 10).

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TREATMENT OF INFERIOR OBLIQUE OVERACTION Surgery is indicated when the inferior oblique overaction and V-pattern interfere with fusion, or if it becomes a cosmetic problem. In general, 2 or more inferior oblique overaction should be considered surgically signiﬁcant whereas 1 or less overaction usually does not require treatment. There are, however, two important exceptions to this rule. The ﬁrst exception is in patients with bilateral asymmetrical inferior oblique overaction in which one eye shows minimal overaction. In these cases, both inferior oblique muscles should be weakened, even if one only shows trace overaction. Unilateral inferior oblique weakening surgery in an asymmetrical bilateral case unmasks the inferior oblique overaction of the nonoperated eye. Inferior oblique surgery should also be considered for bilateral overaction associated with a signiﬁcant V-pattern (Y-subtype), even if there is minimal upshoot on sidegaze. Patients who have a signiﬁcant divergence when the eyes move from primary position to upgaze should have inferior oblique weakening surgery, despite the minimal overaction observed with versions. In most cases, inferior oblique overaction is bilateral and bilateral surgery should be performed. Patients with amblyopia of two lines or greater difference in visual acuity, however, should have monocular surgery, which should be limited to the amblyopic eye to avoid the risk (although slight) of surgical complications to the nonamblyopic eye. When inferior oblique overaction coexists with horizontal strabismus, both should be corrected in the same operation. Staged planning of two separate operations does not improve surgical results and requires a second round of anesthesia. When planning simultaneous horizontal and inferior oblique surgery, the horizontal surgical numbers are not altered. Even though the inferior oblique muscles have an abduction function, weakening the inferior oblique muscles does not signiﬁcantly alter the horizontal alignment unless there is an extremely large V-pattern and severe inferior oblique overaction.

SURGICAL TECHNIQUES FOR WEAKENING THE INFERIOR OBLIQUE MUSCLES (SEE ALSO CHAPTER 11) Surgical techniques for correcting inferior oblique overaction include myectomy, recession, and anteriorization.1,7,19 Recently,

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the anteriorization procedure has become popular, as results have been good even in cases of severe overaction. Anteriorization works by transposing the inferior oblique insertion from its normal position posterior to the equator of the eye to a position anterior to the equator. When the inferior oblique insertion is anterior to the equator, the inferior oblique muscle no longer acts as an elevator but, instead, pulls the front of the eye down; now, it is actually a depressor. This change is why anteriorization procedures that place the inferior oblique muscle anterior to the inferior rectus insertion can cause the complication of an ipsilateral hypodeviation and limited elevation.4,33 This complication can be avoided by keeping the anterior inferior oblique muscle ﬁbers posterior to the inferior rectus insertion. Keeping the posterior ﬁbers of the inferior oblique muscle at least 3 mm posterior to the inferior rectus insertion is especially important because of the inferior oblique neurovascular bundle.34,35 The neurovascular bundle is a relatively inelastic structure inserting in the posterior aspect of the inferior oblique muscle. If the posterior ﬁbers are anteriorized to the level of the inferior rectus insertion, the neurovascular bundle will tighten and act as a tether holding the eye down. Anteriorizing the posterior ﬁbers produces a J-deformity of the inferior oblique insertion. This author prefers avoiding the J-deformity and has developed a graded anterior transposition procedure that keeps the posterior ﬁbers posterior to the anterior ﬁbers. The graded anterior transposition procedure yields excellent results, even in severe cases, without the complication of limited elevation.9 Because the full anteriorization procedure with a J-deformity causes limited elevation, it is rarely indicated. However, it can be considered if performed bilaterally for severe bilateral inferior oblique overaction with a large DVD.

Brown’s Syndrome ETIOLOGY Brown’s syndrome is a restrictive strabismus characterized by limitation of elevation that is worse when the eye is in adduction (Fig. 9-10A). It can be congenital or acquired, with a variety of causes for the restriction of elevation in adduction (see Table 9-7). The term congenital Brown’s syndrome or “true” Brown’s syndrome, is used to refer to Brown’s syndrome caused by a congenitally inelastic superior oblique muscle–tendon complex.36

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FIGURE 9-10A,B. (A) Preoperative composite nine-gaze photograph of patient with congenital Brown’s syndrome, right eye, with limited elevation in adduction and minimal to no superior oblique overaction. Note Y-pattern with exodeviation in upgaze. Also note there is some limitation of the right eye even in abduction, but the limitation is greatest in adduction. Despite the severe limitation of elevation, there is only trace hypotropia in primary position. (B) Postoperative photograph after a Wright’s superior oblique tendon silicone expander, right eye, for Brown’s syndrome. Note the versions are almost normal with only a trace limitation to elevation, which is the optimal result, with a slight residual limitation of elevation in adduction right eye. This was the author’s ﬁrst silicone expander patient, and the results have remained excellent over 11 years of follow-up.

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TABLE 15-7. Classiﬁcation of Brown’s Syndrome. I. Congenital onset A. True congenital Brown’s syndrome (superior oblique etiology) i. Unknown: probable inelastic muscle–tendon complex B. Congenital pseudo-Brown’s syndrome (nonsuperior oblique cause) i. Anomalous inferior orbital adhesions ii. Posterior orbital bands iii. Anomalous insertion of rectus muscle and pulley (e.g., inferior displacement of lateral rectus pulley or insertion) II. Acquired onset A. Superior pblique or trochlear etiology i. Peritrochlear scarring and adhesions 1. Chronic sinusitis 2. Trauma: superior temporal orbit 3. Blepharoplasty and fat removal 4. Lichen sclerosus et atrophicus and morphea ii. Tendon–trochlear inﬂammation and edema 1. Idiopathic inﬂammatory (pain and click) 2. Trochleitis with superior oblique myocytis 3. Acute sinusitis 4. Adult rheumatoid arthritis 5. Juvenile rheumatoid arthritis 6. Systemic lupus erythematous 7. Possibly distant trauma (CPR and long bone fractures) 8. Possibly hormonal changes postpartum iii. Superior nasal orbital mass 1. Glaucoma implant 2. Neoplasm iv. Tight or inelastic superior oblique muscle 1. Thyroid disease (inelastic muscle) 2. Peribulbar anesthesia (inelastic tendon) 3. Hurler–Scheie’s syndrome (inelastic tendon) 4. Superior oblique tuck (short tendon) v. Idiopathic B. Nonsuperior oblique or trochlear causes i. Floor fracture ii. Retinal band around inferior oblique muscle iii. Inferior temporal adhesions Source: From Ref. 32, with permission.

There are nonsuperior oblique causes for congenital Brown’s syndrome, including inferior orbital mechanical restriction, superior nasal orbital mass, and inferior displaced lateral rectus muscle and pulley.22,36

CLINICAL FEATURES OF BROWN’S SYNDROME The hallmark of Brown’s syndrome, regardless of the cause, is limited elevation in adduction. In congenital Brown’s syndrome,

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this occurs because the tight posterior tendon ﬁbers prevent the back of the eye from rotating down; therefore, the front of the eye cannot elevate.36 This restriction is a constant limitation and does not improve or resolve on its own. Typically, on clinical examination, there is minimal to no hypotropia in primary position, minimal to no superior oblique overaction, limited elevation in adduction, and divergence (Y-pattern) in upgaze (Fig. 9-10A).36 There is often some limitation of elevation in abduction, but the key is that the limitation is much worse in adduction.36 Limited elevation in abduction can produce pseudoinferior oblique overaction of the fellow eye because of Hering’s law.36 Intorsion on attempted upgaze has been reported.36 Patients with Brown’s syndrome usually have excellent binocular fusion, as they adopt a compensatory chin elevation and a face turn away from the Brown’s eye to maintain fusion. A patient with a right Brown’s syndrome will have a chin elevation and a face turn to the left. Standard forced-duction testing shows a restriction to elevation in adduction. If the Brown’s syndrome is caused by a tight superior oblique tendon, then Guyton’s exaggerated forcedduction testing of the superior oblique muscle will reveal a restriction to the eye moving up and in.

ACQUIRED BROWN’S SYNDROME Causes of acquired Brown’s syndrome include pathology of the superior oblique tendon and trochlea and nonsuperior oblique pathology.36 Causes for trochlear or tendon abnormalities include repeat upper eyelid blepharoplasty, sinusitis with peritrochlear inﬂammation, rheumatoid arthritis, and a superior nasal mass deﬂecting the course of the superior oblique tendon (e.g., superior nasal glaucoma implant or superior nasal orbital tumor). Inﬂammatory Brown’s syndrome may be idiopathic primary trochleitis or secondary to sinusitis. Acquired nonsuperior oblique or trochlear causes of limited elevation in adduction include ﬂoor fracture, inferior scarring of the globe, fat adherence after inferior oblique muscle surgery, and strabismus surgery with inferior transposition of horizontal rectus muscles (e.g., infraplacement of a lateral rectus resection and medial rectus recession). Furthermore, many patients will develop an acquired Brown’s syndrome of unknown etiology (Table 9-6).

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Idiopathic acquired Brown’s syndrome is often intermittent and sometimes associated with a “click” that is felt by the patient in the superior nasal quadrant when the patient looks up and in. In some cases, the click can be heard with a stethoscope placed in the superior nasal quadrant. The cause of the click and limited elevation is not known, but it may represent inﬂammation or an abnormality of fascial tissue around the superior oblique tendon. If the cause of an acquired Brown’s syndrome is in question, then orbital imaging studies are indicated. In many cases, acquired Brown’s syndrome will spontaneously resolve over several months to even several years. Surgery should only be considered after the patient has been observed for at least 6 months to 1 year. Another form of acquired Brown’s syndrome is inﬂammatory Brown’s syndrome, which is associated with superonasal orbital pain and tenderness. It is hypothesized that trochlear or peritrochlear inﬂammation is the cause. In some cases, inﬂammatory Brown’s syndrome is associated with a concurrent sinusitis36 or rheumatoid arthritis (rarely). In the majority of cases, however, the cause of the inﬂammation is unknown. The treatment of inﬂammatory Brown’s syndrome includes a trial of systemic nonsteroidal antiinﬂammatory agents (e.g., indomethacin 25–50 mg TID) or a local steroid injection in the area of the trochlea. A patient diagnosed with acquired Brown’s syndrome of unknown etiology should undergo workup with orbital imaging, as a variety of local or systemic diseases involving the trochlea may cause a Brown’s syndrome. Medical therapy, not surgery, is the treatment of choice for most cases of inﬂammatory Brown’s syndrome.

CONGENITAL ELEVATION DEFICIT: DIFFERENTIAL DIAGNOSIS Congenital causes for limited elevation include double elevator palsy (see Chapter 10), Brown’s syndrome, inferior oblique paresis, and superior oblique overaction. Double elevator palsy can be distinguished by the presence of similar limitation in abduction and adduction, while primary superior oblique overaction and inferior oblique paresis may be more difﬁcult to differentiate because they have a greater elevation deﬁcit in adduction. See Table 10-6 for a comparison of the clinical ﬁndings of superior oblique overaction, Brown’s syndrome, and inferior oblique paresis.

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SURGICAL INDICATIONS FOR CONGENITAL BROWN’S SYNDROME In general, surgery should be considered for Brown’s syndrome if there is a hypodeviation in primary position that causes a signiﬁcant chin elevation. Patients with a minimal restriction and no signiﬁcant face turn can be managed conservatively. Except for a few exceptions, surgery should be reserved for children older than 4 years of age; older children are less likely to develop postoperative suppression and amblyopia. Rarely, one may be forced to operate on a child under 4 years of age if the hypodeviation is large enough to disrupt fusion.

SURGERY FOR CONGENITAL BROWN’S SYNDROME Management of congenital Brown’s syndrome is based on lengthening the superior oblique tendon.39 Procedures such as tenotomy and tenectomy release the restriction but are not controlled, as the cut ends of the tendon can separate widely and result in a superior oblique paresis. In Brown’s syndrome, the superior oblique muscle is not overacting and, therefore, procedures such as tenotomy or tenectomy often result in a secondary superior oblique paresis. In a study by Eustis et al., 85% of Brown’s patients demonstrated some degree of posttenotomy superior oblique paresis, with one-third requiring a second operation.8 Sprunger et al. reported that 50% of their study patients required further surgery caused by an ipsilateral superior oblique paresis after superior oblique tenotomy.32 To address this problem, Parks has previously suggested performing an ipsilateral inferior oblique recession at the same time as the superior oblique tenotomy. This approach, however, results in prolonged underaction of the inferior oblique and a persistence of Brown’s syndrome. To achieve a controlled elongation of the superior oblique tendon, this author has developed a procedure called the Wright superior oblique tendon expander (see Chapter 11). A segment of retinal silicone band (usually 6.0 mm long) is carefully sutured between the cut ends of the superior oblique tendon, 3 mm nasal to the superior rectus muscle. The initial conjunctival incision, however, is made temporal to the superior rectus muscle. The temporal incision is stretched nasally to expose the nasal aspect of the superior rectus muscle. This maneuver preserves nasal intermuscular septum so the silicone segment does not scar to

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sclera. With the capsule ﬂoor intact, the silicone is actually placed within the superior oblique tendon capsule. Parks, this author, and others have obtained excellent results using the superior oblique tendon expander. The expander allows for controlled and reversible elongation of the tendon while maintaining the functional integrity of the superior oblique muscle–tendon complex. In trained hands, complications of the procedure are rare, but these include extrusion of silicone and scarring of the silicone to the sclera, causing postoperative limitation of depression. These complications can be limited by meticulous technique and limiting the maximum length of the silicone segment to 7.0 mm. Many now consider the superior oblique silicone tendon expander the procedure of choice for Brown’s syndrome.

RESULTS

OF THE

SILICONE TENDON EXPANDER

This author has reported his long-term results using the Wright superior oblique silicone tendon expander on patients with severe Brown’s syndrome (see Fig. 9-10A,B).41 Of 15 patients operated on by the author, preoperative limitation of elevation in adduction measured 3 in 1 patient and 4 in 14 patients. Postoperatively, 14 of the 15 patients showed improved motility with 10 patients demonstrating essentially normal versions. The 1 patient who did not improve after the silicone expander had a nonsuperior oblique tendon cause of Brown’s syndrome. The average final result graded on a scale of 1 to 10 (10 being best) was 8.3. Thirteen (13) of 15 patients (87%) achieved a final result score of 7 or better with a single surgery, and an additional patient was corrected with a second surgery providing an overall success rate of 93%. Ten of the 15 patients had at least 11 months follow-up, with 6 of the 10 patients showing a delayed improvement over a 4- to 6-month period. Five patients had more than 5 years follow-up and 4 (80%) had an excellent long-term outcome (final result, 9–10) with a single operation. All 5 patients had a good outcome (final result, 7–10; mean, 9.2) with 1 patient requiring a second surgery. There were no long-term complications, including no extrusions, no restriction of ocular rotations, and no infections. Stager et al.34 also reported good long-term results; however, in both papers, Wright and Stager emphasized the importance of surgical technique.34,41 Keep the nasal intermuscular septum and the ﬂoor of the superior oblique tendon capsule intact. Also,

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perform the tenotomy at least 3 mm nasal to the superior rectus muscle to avoid adhesions to the superior rectus muscle. Finally, use 5 to 6 mm of silicone band segment for Brown’s syndrome. Both papers also commented on late improvement after surgery. Some patients showed a signiﬁcant undercorrection immediately after surgery, but then improved to have excellent result by weeks, to even months, after surgery. The Wright silicone tendon expander is an effective option for correcting Brown’s syndrome, caused by a stiff or inelastic superior oblique tendon, with excellent long-term outcomes. Proper technique with maintenance of the tendon capsule is critical to the successful outcome of the procedure.43

CANINE TOOTH SYNDROME Scarring in the area of the superior oblique tendon and trochlea will limit movement of the tendon in both directions, resulting in a Brown’s syndrome with a superior oblique paresis. This disorder has been called “Canine tooth syndrome” or Knapp type 7 classiﬁcation.2,14,15,18,21,43 In this author’s thesis43 on Brown’s syndrome, three patients were diagnosed as having Canine tooth syndrome with both restrictive elevation in adduction and a superior oblique palsy. All three cases presented with penetrating trauma to the trochlear area, two by metal hooks and one from a dog bite. Management of these cases is difﬁcult, as surgery in the area of the trochlea can lead to further scarring and worsening of the condition. In the acute phase immediately after trauma, local corticosteroid injection might help reduce secondary ﬁbrosis.2 Initial management is conservative observation because spontaneous improvement may occur.18 If the deviation persists after 4 to 6 months, then surgical correction can be considered. In these cases, it is best to correct the strabismus by operating on the extraocular muscles rather than trying to remove ﬁbrosis in the trochlear area.43

References 1. Apt L, Call NB. Inferior oblique muscle recession. Am J Ophthalmol 1978;95:95. 2. Bachynski BN, Flynn JT. Direct trauma to the superior oblique tendon following penetrating injuries of the upper eyelid. Arch Ophthalmol 1985;103:1510–1514. 3. Berke RN. Tenotomy of the superior oblique for hypertropia. Trans Am Ophthalmol Soc 1946;44:304–342.

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4. Bremer DL, Rogers GL, Quick LD. Primary position hypotropia after anterior transposition of the inferior oblique. Arch Ophthalmol 1986; 104:229–232. 5. Cheng H, Burdon MA, Shun GA, Czypionka S. Dissociated eye movements in craniosynostosis: a hypothesis revived. Br J Ophthalmol 1993;77:563–568. 6. Demer JL. Orbital connective tissue in binocular alignment and strabismus. In: Lennerstrand G (ed) Advances in strabismus research: basic and clinical aspects. London: Portland Press, 2000:17–31. 7. Elliot L, Nankin J. Anterior transposition of the inferior oblique. J Pediatr Ophthalmol Strabismus 1981;18:35. 8. Eustis HS, O’Reily C, Crawford JS. Management of superior oblique palsy after surgery for true Brown’s syndrome. J Pediatr Ophthalmol Strabismus 1987;24:10–16. 9. Guemes A, Wright KW. Effect of graded anterior transposition of the inferior oblique muscle on versions and vertical deviation in primary position. J Am Assoc Pediatr Ophthalmol Strabismus 1998:2:201– 206. 10. Guyton DL. Clinical assessment of ocular torsion. Am Orthopt J 1983;33:7. 11. Harada M, Ito Y. Visual correction of cyclotropia. Jpn J Ophthalmol 1964;8:88. 12. Helveston EM. Classiﬁcation of superior oblique muscle palsy. Ophthalmology 1992;99:1609–1615. 13. Helveston EM. A two-step test for diagnosing paresis of a single vertically acting extraocular muscle. Am J Ophthalmol 1967;64(5): 914–915. 14. Helveston EM, Birchler C. Class VII superior oblique palsy: subclassiﬁcation and treatment suggestions. Am Orthopt J 1982;32:104– 110. 15. Knapp RP. Classiﬁcation and treatment of superior oblique palsy. Am Orthopt J 1974;24:18–22. 16. Kraft SP, Scott WE. Masked bilateral superior oblique palsy: clinical features and diagnosis. J Pediatr Ophthalmol Strabismus 1986;23(6): 264–272. 17. Kushner BJ. The diagnosis and treatment of bilateral masked superior oblique palsy. Am J Ophthalmol 1988;105(2):186–194. 18. Legge RH, Hedges TR III, Anderson M, et al. Hypertropia following trochlear trauma. J Pediatr Ophthalmol Strabismus 1992;29(3):163– 166. 19. Mims JL, Wood RC. Bilateral anterior transposition of the inferior obliques. Arch Ophthalmol 1989;107:41. 20. Muchnick RS, Stoj M, Hornblass A. Traumatic inferior oblique muscle paresis. J Pediatr Ophthalmol Strabismus 1985;22(4):143– 146. 21. Neely KA, Ernest JT, Mottier M. Combined superior oblique paresis and Brown’s syndrome after blepharoplasty. Am J Ophthalmol 1990; 109(3):347–349.

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22. Oh SY, Clark RA, Velez F, Demer JL. Magnetic resonance imaging (MRI) demonstration of instability of rectus pulleys as cause of incomitant strabismus. Investig Ophthalmol Vis Sci 2001;42(4):167. 23. Parks M. Isolated cyclovertical muscle palsy. Arch Ophthalmol 1958;60:1027. 24. Parks MM. The overacting inferior oblique muscle. Am J Ophthalmol 1974;77:787. 25. Parks MM. Bilateral superior oblique tenotomy for A-pattern strabismus in patients with fusion (commentary). Binoc Vis 1988; 3:39. 26. Paysee EA, Coats DK, Plager DA. Facial asymmetry and tendon laxity in superior oblique palsy. J Pediatr Ophthalmol Strabismus 1995;32(3):158–161. 27. Plager DA. Traction testing and superior oblique palsy. J Pediatr Ophthalmol Strabismus 1990;27:136–140. 28. Pollard ZF. Diagnosis and treatment of inferior oblique palsy. J Pediatr Ophthalmol Strabismus 1993;30(1):15–18. 29. Raina J, Wright KW, Lin MM, McVey JH. Effectiveness of lateral rectus Y-split surgery for correcting the upshoot and downshoot in Duane’s retraction syndrome, type III. Binoc Vis Strabismus 1997; 12(4):233–238. 30. Reese PD, Scott WE. Superior oblique tenotomy in the treatment of isolated inferior oblique paresis. J Pediatr Ophthalmol Strabismus 1987;24(1):4–9. 31. Romano P, Roholt P. Measured graduated recession of the superior oblique muscle. J Pediatr Ophthalmol Strabismus 1983;20:134–140. 32. Sprunger DT, von Noorden GK, Helveston EM. Surgical results in Brown’s syndrome. J Pediatr Ophthalmol Strabismus 1991;28(3):164– 167. 33. Stager DR, Weakley DR, Stager D. Anterior transposition of the inferior oblique: anatomic assessment of the neurovascular bundle. Arch Ophthalmol 1992;110:360. 34. Stager DR, Stager D, Parks MM. Long-term results of silicone expander for moderate and severe Brown’s syndrome. J Am Assoc Pediatr Ophthalmol Strabismus 1999;3:328–332. 35. Stager DR. The neuroﬁbrovascular bundle of the inferior oblique muscle as its ancillary origin. Trans Am Ophthalmol Soc 1996;94: 1073–1094. 36. Wright KW. Color atlas of strabismus surgery: strategies and techniques. Torrance, CA: Wright 2000:184–203. 37. Wright KW. Current approaches to inferior oblique muscle surgery. In: Hoyt CS (ed) Focal points 1986: clinical modules for ophthalmologists. Am Acad Ophthalmol 1986;1. 38. Wright KW. Superior oblique silicone expander for Brown’s syndrome and superior oblique overaction. J Pediatr Ophthalmol Strabismus 1991;28:101–107. 39. Wright KW. Surgical procedure for lengthening the superior oblique tendon. Investig Ophthalmol Vis Sci 1989;30(suppl):377.

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40. Wright KW, Min BM, Park C. Comparison of superior oblique tendon expander to superior oblique tenotomy for the management of superior oblique overaction and Brown’s syndrome. J Pediatr Ophthalmol Strabismus 1992;29:92–99. 41. Wright KW. Results of the superior oblique tendon elongation procedure for severe Brown’s syndrome. Trans Am Ophthalmol Soc 2000;98:41–50. 42. Wright KW. Superior oblique silicone expander for Brown’s syndrome and superior oblique overaction. J Pediatr Ophthalmol Strabismus 1991;28:101–107. 43. Wright KW. Brown’s syndrome: diagnosis and management. Trans Am Ophthalmol Soc 1999;97:1023–1109.

10 Complex Strabismus: Restriction, Paresis, Dissociated Strabismus, and Torticollis Kenneth W. Wright

T

his chapter on complex strabismus reviews the evaluation and management of incomitant strabismus associated with rectus muscle paresis and ocular restriction. Other topics include dissociated strabismus complex, torticollis, and nystagmus. Incomitant strabismus is a deviation that changes in different ﬁelds of gaze. Incomitance can be caused by ocular restriction, extraocular muscle paresis, or oblique muscle dysfunction or can be associated with a primary A- or V-pattern. The diagnosis and treatment of oblique muscle dysfunction (palsy and overaction), Brown’s syndrome, and A- and V-patterns are covered in Chapter 9.

PARALYTIC RECTUS MUSCLES AND RESTRICTIVE STRABISMUS: GENERAL PRINCIPLES If an eye has limited ductions, there are only two basic causes: extraocular muscle paresis or ocular restriction. Therefore, a strabismus associated with limited ductions is secondary to extraocular muscle paresis, ocular restriction, or both.

Paresis Extraocular muscle paresis means weak muscle pull, whereas palsy indicates a complete lack of muscle function. Cranial 323

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nerve paresis and primary muscle disease are obvious reasons for a weak muscle that can cause limited ocular rotations. A muscle paresis can also be caused by ineffective muscle pull on the eye, or mechanical disadvantage of muscle pull. Clinical examples of conditions that cause mechanical disadvantage of muscle pull include: • A scarred or tethered muscle preventing transmission of muscle pull to the globe (e.g., ﬂoor fracture with entrapped inferior rectus muscle) • A posteriorly displaced rectus muscle (e.g., slipped muscle) • A muscle shifted out of its appropriate plane, thus diminishing the vector force in the ﬁeld of action of the muscle (e.g., high myopia with displaced lateral rectus muscle) Table 10-1 lists the three major causes of a mus-cle paresis: (1) cranial nerve paresis, (2) primary muscle disease, and (3) mechanical disadvantage of muscle pull. Speciﬁc types of paralytic strabismus, including sixth and third nerve palsies, are covered later in this chapter.

TABLE 10-1. Causes of Muscle Paresis.

a

Cranial nerve palsy

Primary muscle disease

Mechanical disadvantage of muscle pull

Third nerve palsy

Botulism

Fourth nerve palsya (superior oblique palsy) Sixth nerve palsy

Myasthenia gravis

Stretched scar after muscle surgery Slipped muscle or lost muscle

CPEO

Trauma to muscle

Miller–Fisher syndrome (Guillain-Barré)

Cranial nerve aberrant innervation syndromes (e.g., Duane’s syndrome)

Agenesis of an extraocular muscle often associated with a craniofacial disorder

See Chapter 9.

Canine tooth syndrome with scarring of trochlea causing Brown’s syndrome with superior oblique palsy Floor fracture with an entrapped inferior rectus muscle causing limited depression High myopia with large posterior staphyloma, and slippage of lateral rectus below globe reducing lateral rectus abduction force, causing esotropia

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Ocular Restriction Classically, the term ocular restriction describes a mechanical tether or leash that limits ocular rotations. Ocular restriction, however, can be caused by at least two general mechanisms: a mechanical tether on eye movements or misdirected muscle forces that work against the normal agonist muscle function. The term restriction is often loosely used as a general term for limited eye movements; however, a clear distinction should be made between ocular restriction and rectus muscle palsy. If the cause of diminished eye movements is not known, then use the term limited rotations or limitation of eye movements until the etiology is determined. Table 10-2 lists the causes of restrictive strabismus. Mechanical restriction of eye movement is caused by adhesions to an extraocular muscle or sclera, a tight or inelastic extraocular muscle, or an orbital mass. Restrictive adhesions can occur from conjuctival scarring, scarring of Tenon’s capsule, orbital fat adherence, and, rarely, congenital ﬁbrotic bands that attach to the eye or extraocular muscles. Inelastic muscle or muscle ﬁbrosis occurs with thyroid myopathy, local anesthesia myotoxicity, and congenital muscle ﬁbrosis (e.g., monocular elevation deﬁcit and congenital ﬁbrosis syndrome). An orbital mass, such as an orbital hemangioma, or a glaucoma implant can cause ocular restriction either by direct interference of rotation of the eye or by pressure on an extraocular muscle that tightens the muscle. Restriction resulting from misdirected muscle force vectors occurs in conjunction with aberrant innervation of an antagonist muscle and abnormal muscle–pulley location or a displaced extraocular muscle.20,25,83 An example of aberrant innervation causing restriction is limited adduction, often associated with Duane’s syndrome. Restricted adduction occurs because the lateral rectus muscle is aberrantly innervated by part of the medial rectus nerve. When the eye attempts to adduct, the lateral rectus muscles contracts against the contracting medial rectus muscle, thus restricting adduction. An example of displaced extraocular muscle is the V-pattern strabismus and superior oblique muscle underaction that are frequently seen in patients with craniosynostosis.20 These patients have excyclorotation of the orbits that results in superior displacement of the medial rectus muscle and limited ocular depression in adduction. The superiorly displaced medial rectus muscle pulls the eye up in addition to its normal function of

Acquired Brown’s syndrome: scarring or inﬂammation around the trochlea

Thyroid: Graves disease

Congenital ﬁbrosis syndrome

Congenital Brown’s syndrome: inelastic SO muscle tendon complex (see Chapter 9)

SO, superior oblique.

Fat adherence to extraocular muscle (e.g., after strabismus surgery, retinal surgery, or periocular trauma) Monocular elevation deﬁcit syndrome caused by a ﬁbrotic inferior rectus

Entrapped muscle after orbital fracture (inferior rectus most common) Fibrosis after local anesthetic injection into a muscle (inferior most common)

Structural adhesions

Fat adherence to muscle or sclera (e.g., after strabismus surgery, retinal detachment surgery, or periocular trauma) Congenital ﬁbrotic band

Tight extraocular muscle

Mechanical restriction

TABLE 10-2. Causes of Ocular Restriction. Orbital mass

Orbital tumor causing mass effect on globe movement Glaucoma explant with large bleb causing mass effect on globe movement or displace SO tendon (acquired Brown’s syndrome)

High myopia with large posterior staphyloma (Duane’s syndrome)

Misdirected muscle forces

High myopia with large posterior staphyloma and slippage of lateral rectus below globe

Congenital ectopic extraocular muscle insertion and or pulley (craniosynostosis, extorted orbit) Iatrogenic displaced muscle insertion; antielevation after inferior oblique anteriorization with J-deformity, and limited depression after anterior displacement of SO tendon by retinal band

Congenital cranial nerve aberrant innervation

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adduction and limits depression in the ﬁeld of action of the superior oblique.20 A rare example of restriction caused by a displaced muscle–pulley was reported by Oh et al.83 They described a patient with limitation of elevation in adduction, or a pseudoBrown’s syndrome, caused by a congenitally inferiorly displaced lateral rectus muscle and its pulley. These authors hypothesized that the infraplaced lateral rectus muscle and pulley act to pull the eye down, limiting elevation on adduction. Iatrogenic displacement of extraocular muscles during strabismus surgery can also cause limited eye movements. Inferior oblique muscle anteriorization anterior to the inferior rectus insertion can also cause active restriction and limited elevation (see Chapter 2, Fig. 2–17).15,43,114,135 In some cases, restriction and paresis coexist, such as with paretic lateral rectus muscle and secondary contracture of its antagonist medial rectus muscle. It is important to diagnoses the cause of limited ductions to formulate an effective surgical plan. The next section describes methods for diagnosing extraocular muscle paresis and ocular restriction.

Diagnosing Restriction Versus Paresis The principal diagnostic tests that differentiate paresis from restriction include saccadic velocity measurements, forced ductions, and forced-generation test. Other signs inﬂuencing diagnosis include intraocular pressure changes in various ﬁelds of gaze and lid ﬁssure changes in sidegaze.

SACCADIC VELOCITY MEASUREMENTS Saccadic velocity measurements can help differentiate restriction from paresis by observation, without touching the eye. Therefore, this method is useful in young children as well as adults. Saccadic movements are fast, jerk-like eye movements that require normal rectus muscle function. The rectus muscles are the major movers of the eye and are responsible for saccadic eye movements. The presence of a saccadic eye movement indicates normal rectus muscle function whereas the inability to stimulate a saccade suggests a rectus muscle palsy. A paretic rectus muscle does not have the power to generate a saccadic eye movement, and the eye drifts slowly to the intended ﬁeld of gaze. Strabismus associated with limited ductions and diminished saccadic velocity is caused by a rectus muscle paresis, not an oblique muscle palsy.

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In contrast to a rectus muscle paresis, ocular restriction is associated with normal, but shortened, saccadic movements as the eye stops abruptly when the restriction is met. This eye movement pattern of a fast eye movement that stops abruptly as it meets the restriction is termed the dog on a leash; it is analogous to a dog lunging after a cat, then being abruptly stopped by its leash (Fig. 10-1). In patients with limited eye movements, it is important to clinically test for saccadic eye movements before surgery to assess muscle function. At the time of surgery when the patient is under anesthesia, it is impossible to test muscle function. Positive forced ductions at the time of surgery indicate only passive restriction and do not exclude the possibility of coexisting muscle palsy. Horizontal and vertical eye movements can be measured by laboratory tests including electro-oculogram (EOG) recordings and infrared eye trackers. Clinical observation of eye movements can also be used in clinical practice for evaluating the presence of a saccadic movement; this is facilitated through the use of an optokinetic nystagmus (OKN) drum for young children who are not able to follow instructions as well as for cooperative patients to compare eye movements (Fig. 10-2). Rotate the OKN drum and observe the patient’s eyes for a brisk redress

FIGURE 10-1. “Dog on a Leash.” The pattern of a fast eye movement that stops abruptly indicates a mechanical restriction. Upper: cartoon shows a dog on a leash walking toward a cat behind a tree. Lower: The dog sees the cat and leaps for the cat but is stopped abruptly by the leash.

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FIGURE 10-2. Photograph of a child being examined with an optokinetic nystagmus (OKN) drum. The saccadic movement will be in the direction opposite to the drum rotation. This is a good clinical method to estimate if a saccade is present.

movement opposite to the direction of the drum rotation. Compare eye to eye and look for asymmetry of the OKN response. An inability to generate a saccadic movement indicates a paretic rectus muscle.

FORCED DUCTIONS Forced ductions identify the presence of a mechanical restriction to ocular rotation; these are performed by grasping the eye with a forceps and then passively moving the eye into the ﬁeld of limited ocular rotation. If the eye shows a resistance to rotation with the forceps (positive forced ductions), then there is a mechanical restriction. When performing forced ductions for possible rectus muscle restriction, proptose the eye to stretch the rectus muscles. This maneuver will allow identiﬁcation of restriction caused by a tight rectus muscle. If the examiner inadvertently retropulses the eye, the rectus muscles slacken and produce a negative forced-duction test, even if the rectus muscle is tight (Fig. 10-3). The opposite holds true for oblique muscle forced ductions, because retropulsing the eye will stretch the oblique muscles and accentuate a tight oblique muscle. If a restriction is worse with retropulsion of the eye, then the restriction is not caused by a tight rectus muscle but, instead, is

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A B FIGURE 10-3A,B. (A) The proper technique for rectus muscle forced ductions includes grasping the conjunctiva with a 2 3 Lester forceps at the limbus, just anterior to the muscle insertion. First, proptose the eye, and then pull the eye away from the muscle being tested, thus placing the rectus muscle on stretch. This maneuver allows identiﬁcation of even mildly tight or restricted muscles. (B) The improper technique for rectus muscle forced ductions shows the eye being retropulsed during the maneuver, causing iatrogenic slackening of the muscle and a false-normal forced-ductions test. Positive forced ductions that do not improve when the eye is intentionally retropulsed suggest the presence of a nonrectus muscle restriction, such as periocular scarring (e.g., fat adherence).

secondary to either a periocular adhesion or a tight oblique muscle. Forced-duction testing can be used as an in-ofﬁce test using topical anesthesia, or at the time of strabismus surgery. In most cases, the pattern of the eye movements, including the clinical evaluation for saccades, establishes the diagnosis of restriction or paresis. Therefore, in-ofﬁce forced-duction testing is usually not necessary. If surgery is indicated, forced- duction testing can be performed at the time of surgery to verify the diagnosis. It is important to remember that positive forced ductions does not exclude the presence of a coexisting palsy. In fact, most cases of long-standing rectus muscle palsy also have contracture of the antagonist muscle, so forced ductions will be positive. Preoperative evaluation of muscle function by saccadic eye movement

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testing or the forced-generation test (see next section) is required to diagnose a rectus muscle palsy.

FORCED-GENERATION TEST The forced-generation test directly measures active muscle force and is useful for diagnosing a rectus muscle palsy. To perform this test, the eye is topically anesthetized and grasped with forceps; the patient is asked to look into the ﬁeld of limited rotation. A sterile cotton-tipped applicator can also be used to push against the eye to feel the abduction force, as noted in Chapter 5 (Fig. 5-16A,B). The examiner feels the pull of the muscle against the forceps or cotton-tipped applicator and compares this to the fellow eye or the antagonist muscle. If there is diminished pull from the muscle into the ﬁeld of limited rotation, then a paresis is present. Forced ductions can be used in conjunction with forced-generation testing. If forced ductions are positive and the force-generation test shows poor muscle function, then the diagnosis is a combination of restriction and paresis.

INTRAOCULAR PRESSURE CHANGE ON EYE MOVEMENT Another sign of restriction is increased intraocular pressure on attempted duction into the ﬁeld of limited movements and away from a restriction or tight muscle. Intraocular pressure increases as the eye forcibly attempts to move against the restriction. Patients with thyroid myopathy and strabismus may show increased intraocular pressure when the pressure reading is made with the restricted eye in forced primary position.

LID FISSURE CHANGES ON EYE MOVEMENT Ocular restriction caused by a tight rectus muscle or a restrictive adhesion to the globe will cause globe retraction and lid ﬁssure narrowing as the agonist rectus muscle attempts to pull the eye away from the restriction [see Duane’s syndrome (Fig. 10-12), later in this chapter]. These movements occur because the eye is restricted from rotating; therefore, the contracting agonist muscle pulls the eye posteriorly and causes globe retraction and lid ﬁssure narrowing. A rectus muscle paresis will cause the opposite: lid ﬁssure widening and relative proptosis. As the patient looks into the ﬁeld of action of the paretic rectus muscle, the agonist muscle relaxes secondary to the palsy. The antagonist muscle also relaxes because of

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Sherrington’s law, and pressure from orbital fat pushes the eye forward. A patient with a sixth nerve palsy, for example, will show lid ﬁssure widening on attempted abduction (see Fig. 10-10, later in this chapter). This change occurs because the medial rectus muscle relaxes on attempted abduction (Sherrington’s law) and, along with the paretic lateral rectus, it is loose; therefore, the posterior pressure of the orbital fat pushes the eye forward.

MANAGEMENT OF INCOMITANT STRABISMUS: GENERAL PRINCIPLES Management begins with understanding why the deviation is incomitant. For example, if an incomitant strabismus is associated with severe limitation of ductions, determine whether the limitation is caused by restriction or paresis. If a signiﬁcant restriction is the cause of limited adduction, then one must release the restriction. If severe limitation of ocular rotations is secondary to poor rectus muscle function, then one has to address the muscle weakness. In cases in which the incomitance is associated with little or no limitation of eye movements, the incomitance can be managed by operating on the good eye to match ocular rotations of the deviated eye. Determine where the deviation is greatest and operate to achieve alignment in primary position while reducing the incomitance. Use this strategy: recession procedures have their greatest effect in the ﬁeld of action of the recessed muscle, and resections produce a leash with the greatest effect occurring when the eye rotates away from the resected muscle (see Chapter 11). Recessing the right medial rectus muscle will produce an exodeviation greater in leftgaze and almost no effect in rightgaze, and resecting the right lateral rectus muscle produces an exodeviation that increases in leftgaze. With this strategy in mind, determine what surgery would best correct the following strabismus. Example 1. Trace limitation of abduction of unknown etiology, left eye; negative forced ductions.

Right ET2 ET, estropia.

Primary

Left

ET 8

ET 16

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The surgical plan is to recess the right medial rectus muscle 4.0 to 5.0 mm, as this will match the right medial rectus muscle to its underacting yoke muscle, the left lateral rectus muscle. Weakening the right medial rectus muscle will slightly reduce adduction but will not affect abduction; this reduces the large esotropia in leftgaze without causing an exotropia in rightgaze. Do not recess the left medial rectus muscle because this surgery has little effect in leftgaze where the esotropia is largest and will produce an exo-deviation in rightgaze. Also, avoid a left lateral rectus resection as this will not strengthen the weak lateral rectus. Instead, it will cause a tight lateral rectus muscle that also has little effect in leftgaze where the esotropia is greatest and will cause an exodeviation in rightgaze. For an incomitant esodeviation that is greater than 10 to 15 prism diopters (PD) in primary position and increases in leftgaze, two-muscle surgery will be required to correct the deviation in primary position. Consider asymmetrical bilateral medial rectus recessions, with a larger recession on the right medial rectus muscle. The Faden operation has also been suggested to reduce incomitance. Adding a Faden to a recession of the medial rectus muscle increases the weakening effect of the recession in adduction and improves the incomitance. The use of the Faden is controversial. If it is used, it is most effective on the medial rectus muscle, as the medial rectus has the shortest arc of contact. Theoretically, the Faden weakens the muscle mostly in the ﬁeld of action of the muscle, with little effect in primary position; therefore, it may be helpful in reducing incomitance (see Chapter 11). A report on the effect of the Faden procedure on the medial rectus muscles in reducing the AC/A ratio concluded there was a beneﬁcial effect; however, the table of data in this study showed no change of the AC/A ratio. It is likely the Faden procedure has little effect, except in extreme ﬁelds of gaze.35 If the limitation is severe, recessing the yoke muscle to match the limitation will not work, as operating on the good eye will not improve the ability of an eye with limited ductions to come to midline. In these cases of moderate to severe limitation of ductions, one must release the restriction or, in the case of a palsy, transpose muscle forces to bring the eye to midline. Recessing the contralateral yoke muscle only works if the limitation is slight, such as a trace to 1 limitation of ductions. Vertical incomitance can be treated with the same strategy as described previously for horizontal strabismus. One special situation that occurs with Grave’s disease and ﬂoor fractures is

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that of a patient with orthotropia in primary position and a hypotropia in upgaze secondary to a tight inferior rectus muscle. In this case, recess both inferior rectus muscles, with a larger recession on the side with the restriction. The diagnosis and management of speciﬁc types of restrictive and paralytic strabismus follow.

SPECIFIC TYPES OF RESTRICTIVE STRABISMUS Fat Adherence Fat adherence is a restrictive form of strabismus occurring after periocular surgery or accidental trauma. Marshall Parks was the ﬁrst to describe the clinical characteristics and etiology of the fat adherence syndrome or, as it is also called, the adhesive syndrome.84 Normally, Tenon’s capsule and muscle sleeve act as an elastic barrier separating the globe from the surrounding orbital fat. Fat adherence is caused by violation of the posterior Tenon’s capsule, allowing exposure and manipulation of extraconal fat and fascia, which produces an adhesion of these tissues to the sclera. Because the septae within the extraconal fat connect to the periorbita, ﬁbrosis associated with fat adherence can extend from the orbital bone to the sclera (Fig. 10-4). In severe cases, the eye is virtually scarred to the orbital bone, immobilizing ocular rotations. Violation of the muscle sleeve can also result in fat adherence to a rectus muscle causing a tight muscle. Fat adherence most frequently occurs after strabismus surgery involving posterior exposure (especially oblique muscle surgery) and retinal buckle surgery, but can also occur after any periocular surgery, even after blepharoplasty.57,59,134 Fat adherence is difﬁcult to surgically correct, as recurrence of fat adherence after removal of adhesions is very common. Once Tenon’s capsule is violated and a scar established, it is almost impossible to reestablish the delicate fascial barrier to prevent recurrence of scarring. Teﬂon or silicone sheaths have been used as an artiﬁcial barrier, but they become encapsulated in scar and often make the restriction worse. Amniotic membrane transplantation has been used to create a barrier separating periocular fat from the sclera, but the technique is difﬁcult, at best, and remains investigational.138 Surgical correction of fat adherence consists of releasing the scar by dissecting close to

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A

FIGURE 10-4A,B. Fat adherence syndrome. (A) Diagram on the right shows the normal anatomy of the periocular fascia with Tenon’s capsule as the barrier separating orbital fat from the sclera and muscle. Diagram to the left shows fat adherence (after violation of Tenon’s capsule) overlying the rectus muscle in an area away from the rectus muscle over sclera. Note that a ﬁbrous scar extends throughout the fat septae attaching periosteum to the muscle and sclera. This scar causes a restrictive leash that limits eye movements. (B) Photograph of fat adherence to the inferior rectus muscle. (Modiﬁed from Parks and Mitchell, 1978, with permission.)

sclera and removing the adhesions without repenetrating the orbital fat. (Perform forced ductions after freeing adhesions to evaluate improvement of the restriction.) Dissect carefully with direct visualization, as posterior dissections can be dangerous.

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Cases of inadvertent optic nerve transection have occurred, although they are rarely reported. If fat and scar are adherent to a rectus muscle, remove a small amount of the anterior scar, then recess the tight muscle en bloc with the scar rather than trying to dissect all the scar off the muscle. Avoid extensive dissection of scar off the muscle, as this usually results in further fat manipulation and worsening of the adherence. Medical treatment with mitomycin-C has not been effective in reducing postoperative ﬁbrosis and may even increase scarring.17 Injection of peribulbar corticosteroids also fails to prevent postoperative scarring. The best treatment for fat adherence syndrome is prevention: avoid penetration of posterior Tenon’s capsule during the initial surgery. During strabismus surgery, perform minimal dissection of muscle fascia and, when dissecting, dissect close to the muscle to stay away from surrounding orbital fat. If Tenon’s capsule is inadvertently torn so fat is exposed, cover the exposed fat by repairing the Tenon’s tear with 7-0 vicryl suture.

Grave’s Ophthalmopathy Grave’s ophthalmopathy is an autoimmune disease associated with inﬂammation of the extraocular muscles. Initially, there is an acute phase during which there is a lymphocytic inﬁltration of the extraocular muscles, resulting in extraocular muscle enlargement and proptosis. This active phase usually lasts several months to more than a year. Orbital imaging studies show thickened extraocular muscles, especially posteriorly. The second phase is a cicatricial phase with quiescence of inﬂammation and secondary contracture of the muscles. All muscles are usually involved, but the inferior rectus and medial rectus are most severely affected.91 Strabismus is caused by tight ﬁbrotic muscles and can develop in both phases but is most pronounced in the cicatricial phase. A restrictive hypotropia caused by tight inferior rectus muscles is the most common type of strabismus, followed by esotropia associated with tight medial rectus muscles. The management of Grave’s ophthalmopathy is careful observation during the acute inﬂammatory phase. Treatment with systemic steroids and even external beam radiation may be indicated for severe disease; however, radiation therapy is not effective for treatment of the strabismus.126 Orbital decompression is indicated for severe proptosis and visual loss associated

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with optic nerve compression from inﬂamed extraocular muscles. In most cases, it is better to perform strabismus surgery after the active phase has subsided and strabismus measurements have stabilized. A report on eight patients whose eyes were operated on during the active phase of thyroid ophthalmopathy noted that all eight patients achieved successful longterm alignment (16 months follow-up); however, half the patients required more than one operation. Regarding the timing of surgery, strabismus surgery is usually performed after orbital decompression surgery, because orbital surgery can alter eye alignment.21,75 The strategy for the treatment of Grave’s ophthalmopathy strabismus is to release the restriction from the tight rectus muscle, with a rectus muscle recession being the procedure of choice. It is not advisable to use rectus muscle resections, as this tightens an already stiff, inelastic muscle. A right hypotropia less than 15 PD with a tight right inferior rectus muscle can be surgically addressed with a right inferior rectus recession, with or without an adjustable suture technique (Fig. 10-5).8,68 If the deviation in primary position is greater than 18 to 20 PD with severe restriction, recess the tight inferior rectus muscle more than 5.0 mm and add a recession of the contralateral superior rectus muscle. As a rule, expect 3 PD of vertical correction for each millimeter of vertical rectus muscle recession.135 One common problem with correcting thyroid strabismus has been late overcorrection after inferior rectus recession, which occurs in up to 50% of cases.24,56,80 Initially after surgery, there is a successful result. Then, at 4 to 6 weeks after the inferior rectus recession, a consecutive hypertropia on the side of the recession occurs, with underaction of the recessed inferior rectus muscle and ipsilateral lower eyelid retraction.132 R. Friedman suggested that performing asymmetrical bilateral inferior rectus recessions avoids late overcorrection. A report by Cruz and Davitt on eight patients who underwent asymmetrical bilateral inferior rectus recessions showed no overcorrections; however, 25% of these patients were undercorrected.24 Ludwig has suggested that a stretched scar at the new insertion is the cause of the overcorrection. It is hypothesized that, at 4 to 6 weeks after surgery, the absorbable suture loses its strength. The muscle–scleral attachment stretches and causes the tight muscle to retract posteriorly. This author has now switched to nonabsorbable sutures (6-0 Mersiline), and preliminary results have been good, even when using an adjustable suture.

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A

B FIGURE 10-5A,B. Thyroid-associated strabismus. (A) Patient with Graves’ disease and limited elevation, right eye, secondary to a tight right inferior rectus muscle. (B) CT scan shows thyroid-associated changes; the medial inferior and superior rectus muscles are enlarged bilaterally.

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Congenital Fibrosis of the Extraocular Muscles Congenital ﬁbrosis of the extraocular muscles (CFEOM) is an autosomal dominant, nonprogressive disorder usually characterized by bilateral congenital ptosis and restrictive external ophthalmoplegia48,49; however, rare unilateral cases have been described (CFEOM 8, 21, 26, 29, 30, 31).28,51 Systemic diseases reported to be associated with CFEOM include Prader–Willi syndrome (CFEOM 25),60 Joubert syndrome (CFEOM 23),3 and cortical and basal ganglia dysplasia (CFEOM 2).123 CFEOM has been mapped to chromosomes 12, 11, and 16 (CFEOM 3, 5, 6, 7, 9, 18, 16).26,51 There can be signiﬁcant phenotypic heterogeneity with a variety of subtypes of CFEOM found in the same family (CFEOM 6 and 8).96,118 The clinical features of CFEOM have been classiﬁed into ﬁve groups: (1) generalized ﬁbrosis syndrome,4 (2) ﬁbrosis of inferior rectus with blepharophimosis, (3) strabismus ﬁxus, (4) vertical retraction syndrome,39 and (5) unilateral ﬁbrosis blepharoptosis and enophthalmos (CFEOM 17).32,34,51 The medial rectus muscle is one of the most commonly involved, causing a strabismus ﬁxus esotropia with extreme restriction to abduction (Fig. 10-6). Strabismus ﬁxus is a term for an eye that is ﬁxed and cannot move, usually secondary to severe restriction or a combination of restriction and paresis. The strabismus associated with CFEOM is mostly caused by tight ﬁbrotic muscles, but a component of paresis can also be a factor. As with thyroidrelated strabismus, the surgical procedure of choice is a recession of the tight rectus muscle. Resections should be avoided. These CFEOM cases can be technically difﬁcult because exposure of the muscle is limited, especially in cases with a ﬁbrotic medial rectus muscle. The etiology of CFEOM is unknown, but the syndrome is associated with atrophic and ﬁbrotic changes of the extraocular muscles.33 Light and electron microscopy demonstrated replacement of normal muscle with collagen, dense ﬁbrous tissue, and areas of degenerated skeletal muscle (CFEOM 29, 30, 31).125 Research suggests that the cause of congenital ﬁbrosis of the extraocular muscles is an abnormality in the development of the extraocular muscle lower motor neurons, with agenesis of the third nerve being most common (CFEOM 1, 14, 11, 10).109 Nakano et al. reported ﬁnding three mutations in ARIX gene (also known as PHOX2A) in four pedigrees of congenital ﬁbrosis of the extraocular muscles type 2 (CFEOM 2).79,123 ARIX

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FIGURE 10-6. Patient with congenital ﬁbrosis syndrome and a large angle esotropia. There was severe limitation to abduction, bilaterally, and forced ductions at the time of surgery show severe restriction to abduction in both eyes. Bilateral medial rectus recessions (7.0 mm) resulted in good alignment with improved abduction.

encodes a homeodomain transcription factor protein shown to be required for development of cranial nerves III and IV in mouse and zebraﬁsh. These ﬁndings conﬁrm the hypothesis that CFEOM 2 results from the abnormal development of cranial nerves III and IV and emphasize a critical role for ARIX in the development of these midbrain motor nuclei.37,79

Double Elevator Palsy or Monocular Elevation Deﬁcit Syndrome Double elevator palsy is classically deﬁned as a congenital inability to elevate one eye, with the limitation occurring in adduction and abduction (Fig. 10-7). One might question why double elevator palsy is included under restrictive strabismus. The term double elevator palsy is a misnomer because, in most cases, the cause for the limited elevation is not a palsy of both elevators but is a tight inferior rectus muscle. Studies using saccadic velocity measurements and forced ductions showed that approximately 70% of patients diagnosed as having a double elevator palsy actually had limited elevation as a result of inferior rectus restriction, not a palsy of the superior rectus and inferior

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oblique muscles.73,106 A more descriptive term now used is monocular elevation deﬁcit syndrome (MED). MED may be mistaken for Brown’s syndrome, although the limited elevation is worse in adduction than abduction in the latter. Patients with MED present with a hypotropia, a chin elevation, and, often, an ipsilateral ptosis. True congenital ptosis is present in 25% of cases whereas pseudo-ptosis may occur in almost all patients with a large hypotropia.2 In those cases with a true double elevator palsy and a lack of an upgaze saccade, forced ductions at time of surgery usually reveal a tight inferior rectus muscle coexisting with the superior rectus palsy. An interesting ﬁnding in approximately 25% of patients with double elevator palsy and congenital ptosis is the Marcus Gunn jaw-winking phenomenon.133 This association indicates a congenital misdirection syndrome involving the oculomotor nerve. It is possible that, as with congenital ﬁbrosis syndrome, the cause of the tight inferior rectus and, in some cases, superior rectus and inferior oblique palsy, is abnormal development of cranial nerves (including the oculomotor nerve) with secondary muscle ﬁbrosis. Surgery for MED is indicated if a signiﬁcant hypotropia is present in primary position with an associated chin elevation. The type of surgery depends on the cause of the elevation deﬁcit (Table 10-3). If the etiology is a tight inferior rectus muscle and the upgaze saccade is normal, recess the ipsilateral inferior rectus muscle, usually around 5 to 6 mm depending on the size of the hypotropia. It is important to evaluate preoperatively for the presence of an upgaze saccade and to perform forced ductions at the time of surgery to make the correct procedural choice. Lack of upgaze saccades, combined with a weak superior rectus muscle on forced generation testing, indicates a true

A B C FIGURE 10-7A–C. Double elevator palsy (monocular deﬁcit syndrome). Child has had limited elevation of the right eye since birth. Note that elevation of right eye is worse in abduction (A) than it is in adduction (C). Patient is ﬁxing with the involved right eye so the left eye is hypertropic as per Hering’s law of yoke muscles (B). Preoperatively, this patient had intact upgaze saccades and a tight inferior rectus muscle on forcedduction testing at the time of surgery. The elevation deﬁcit was successfully treated with a right inferior rectus muscle recession of 6.5 mm.

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TABLE 10-3. Treatment of Double Elevator Palsy (Monocular Elevation Deﬁcit Syndrome). • Tight inferior rectus muscle: good superior rectus function Recess ipsilateral inferior rectus muscle (5–6 mm) • Superior rectus palsy Recess ipsilateral inferior rectus muscle and ipsilateral transposition of half the medial and lateral rectus muscles up to the superior rectus insertion (preferred by author) or Knapp procedure: full-tendon transfer up to the superior rectus muscle

double elevator palsy. In these cases, a recession of the ipsilateral inferior rectus will not correct the hypotropia. Treatment of a true double elevator palsy with weak superior rectus muscle is to perform a transposition of the ipsilateral medial and lateral rectus muscles up to the superior rectus muscle. In patients with the superior rectus palsy type of MED, forced ductions are often positive, and the ipsilateral inferior rectus muscle should be recessed. This author prefers the partial tendon transfer (Hummelsheim) instead of the full-tendon transposition (Knapp) to avoid the possible complication of anterior segment ischemia that can occur up to 20 years after strabismus surgery. In severe cases of hypotropia over 15 PD, consider adding a recession of the contralateral superior rectus muscle.

Orbital Floor Fracture Signs of a blowout fracture include diplopia secondary to restricted vertical eye movement, enophthalmos, and numbness of face below the traumatized orbit and along the upper teeth. Restrictive strabismus with limited elevation in orbital ﬂoor fractures is caused by entrapment of fat and the inferior rectus muscle at the fracture site (Fig. 10-8). Repair of the ﬂoor fracture in most cases will improve ductions. In addition to limited elevation, there can be limited depression on the side of the fracture, often associated with a posterior fracture.108 The cause of the limited depression could be contributed to scarring of the inferior rectus to the ﬂoor, thus preventing the inferior rectus muscle from transmitting its contractual pull to the globe. Adherence of the inferior rectus to the ﬂoor would also isolate the muscle anterior to the fracture and cause the anterior muscle to slacken on attempted downgaze, producing pseudoinferior rectus palsy. These patients characteristically have a small

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hypertropia in primary position, underaction of the inferior rectus muscle, and a large hypertropia in downgaze. The key to the diagnosis of a pseudoinferior rectus palsy is normal inferior rectus muscle function and normal saccades when the eye moves from upgaze to primary position, with inferior rectus muscle weakness and slow ocular movements from primary position to downgaze. Treatment of pseudoinferior rectus palsy is to repair the ﬂoor fracture. If this does not relieve symptoms, then strabismus surgery is indicated. This author has found that a small (3–4 mm) ipsilateral inferior rectus muscle tightening procedure (Wright plication or resection) helps to eliminate the anterior muscle slack. A contralateral inferior rectus recession works well and produces only a slight limitation of elevation. If the muscle is captured in a trap-door fracture, direct damage to the inferior rectus muscle occurs and can truly weaken the inferior rectus muscles. Small trap-door ﬂoor fractures can pinch and strangle the inferior rectus muscle, causing necrosis and muscle damage.11 Because of the potential for permanent damage, some advocate immediate repair within the ﬁrst few days if there is imaging evidence that the inferior rectus is entrapped.29 Strabismus surgery should be performed after reconstructive orbital surgery. If orbital reconstruction is not indicated, and the patient has persistent diplopia 4 to 8 weeks after the trauma, then strabismus surgery is indicated. The strabismus surgical plan depends on the pattern of the strabismus. Table 10-4 lists patterns of strabismus and their associated treatment.

Myotoxic Effect of Local Anesthetics Injection of local anesthetics such as lidocaine and marcaine into an extraocular muscle can result in myotoxic damage to the muscle and cause strabismus.19,40,46 Elderly patients are especially susceptible to the myotoxic effects of local anesthetics. Immediately after the injection of a local anesthetic into an extraocular muscle, there is an acute paresis of the muscle that lasts for one to several days. Over the next few weeks, localized segmental intramuscular ﬁbrosis occurs secondary to local myotoxicity of the anesthetic. The ﬁbrosis results in a tight and contracted muscle. What is particularly interesting is that, in some cases, the injected muscle overacts, producing a deviation that increases in the ﬁeld of action of the injected muscle.8,13 This deviation is in contrast to the restriction pattern usually

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A

B FIGURE 10-8A–B. Orbital ﬂoor fracture left eye with entrapment of fat and the inferior rectus muscle. (A) In primary gaze, there is no signiﬁcant deviation. (B) Restricted elevation of left eye in upgaze causes a large right hypertropia.

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C FIGURE 10-8C. (C) CT scan shows herniation and entrapment of inferior orbital fat into the maxillary antrum. Note that, after removal of the fat and repair of the fracture, the restriction resolved.

expected with a tight muscle, where the deviation is greatest in the gaze opposite to the ﬁeld of the muscle’s action. The cause of the muscle overaction is thought to be secondary to intramuscular ﬁbrosis, with stretching of the Z-bands and enhancing

TABLE 10-4. Orbital Floor Fracture: Surgical Plans. Tight inferior rectus muscle (hypotropia) • Small hypotropia (8 PD) in primary position, no deviation in downgaze, and larger hypotropia in upgaze (tight inferior rectus muscle): Asymmetrical bilateral inferior rectus muscle recessions, with a larger ipsilateral recession Add a contralateral superior rectus recession for a large hypotropia in upgaze • Large hypotropia in primary position, worse in upgaze (tight inferior rectus muscle): Hypotropia 8 to 15 PD: recess ipsilateral inferior rectus muscle (3.5–5.0 mm) Hypotropia 15 PD: recess ipsilateral inferior rectus muscle (5–6 mm) PLUS a contralateral superior rectus recession (4–6 mm) Pseudoinferior rectus muscle palsy (hypertropia) • Hypertropia in primary position increases in downgaze with ipsilateral limited depression; intact saccades from upgaze to primary position: Plication of the ipsilateral inferior rectus (3 mm) PLUS contralateral inferior rectus recession (4–5 mm)

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the action and myosin interaction.19 The ﬁbrosis acts to stretch the muscle ﬁbers that subsequently increases their force, per the Starling’s length tension curve.19 For example, inadvertent injection of the inferior rectus muscle associated with a retrobulbar injection of anesthetic initially results in an ipsilateral hypertropia because of an inferior rectus paresis. Over a few weeks, this changes into an ipsilateral hypotropia with overaction of the inferior rectus muscle, resulting in the hypertropia being greatest in downgaze. Any of the extraocular muscles can be inﬁltrated during a retrobulbar or peribulbar injection of local anesthetics, with the superior and inferior rectus muscles most commonly affected. One of the ﬁndings is segmental enlargement of the injected muscle seen on orbital imaging. Hamed and Mancuso46 reported on eight patients with an ipsilateral hypotropia after a retrobulbar injection of anesthetic, with three patients showing segmental enlargement of the inferior rectus muscle. The treatment is to recess the tight or overacting muscle. This method has produced excellent results, especially in the cases involving an overacting injected muscle, with the deviation larger in the ﬁeld of action of the muscle. One can help prevent intramuscular injection injury by injecting into the orbital quadrant away from the extraocular muscles, using a blunt cannula and limiting anesthetic volume. The incidence of strabismus after cataract surgery has diminished dramatically since the widespread use of topical anesthesia during surgery.

Strabismus After Retinal Surgery Strabismus can occur virtually after every known retinal surgical procedure.38,57,71,72,103,111,114 The strabismus is usually transient; however, persistent strabismus occurs in approximately 7% of scleral buckling procedures.71,117 Common causes of strabismus after retinal detachment surgery include fat adherence and restriction, a lost or slipped muscle, a displaced superior oblique tendon, a large explant under a rectus muscle, and ectopic fovea.38,47,57,85,110 Other causes of strabismus after retinal surgery include patients with preexisting strabismus before the retinal surgery who then experience sensory strabismus secondary to loss of vision.92,130 Of all the causes of persistent restriction after retinal detachment surgery, fat adherence and periocular scarring is by far the most common and most difﬁcult to treat.1,57,134 Fat adherence is difﬁcult to treat because there

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is no synthetic substitute to recreate the natural boundary between the orbital fat and the eye and muscle once Tenon’s capsule is violated. Occasionally, a lost muscle is associated with postretinal surgery, as can occur when the traction sutures around the muscle are pulled to gain posterior exposure during the retinal surgery. In elderly patients, the muscle is relatively weak, and overzealous traction on the rectus muscle can result in a splitting of the muscle; this has been termed pulled-in-two syndrome (PITS). Spontaneous disinsertion and posterior slippage of a rectus muscle behind an encircling buckle can also occur, without removal of the muscle at the time of retinal surgery.47,57 In these cases, the silicone band will cheese-wire through the muscle insertion over several months postoperatively, resulting in late slippage of the muscle behind the buckle and causing an underaction of the slipped muscle. The slipped rectus muscle can almost always be found attached to sclera at the posterior edge of the encircling buckle or connected to sclera by a pseudotendon. Appropriate treatment is to advance the muscle and reattach the muscle with nonabsorbable suture. Another cause for strabismus after retinal surgery is an oblique muscle that has been displaced anteriorly by an encircling band.57,72 Placement of the band behind the superior oblique tendon pulls the superior oblique tendon anteriorly to the nasal aspect of the superior rectus insertion. The superior oblique tendon now inserts at the nasal side of the superior rectus insertion, anterior to the equator. The new anterior insertion of the superior oblique tendon changes the action of the superior oblique muscle from a depressor to an elevator. These patients typically present with a hypertropia and limitation of depression of the involved eye. Forced ductions, however, show relatively mild restriction to depression as compared to the limitation on ductions and versions. Treatment is to release the entrapped superior oblique tendon from the buckle or, if there is severe scarring, perform a superior oblique tenotomy. If the hypertropia is greater than 5 PD in primary position, also perform a recession of the contralateral inferior rectus muscle (consider adjustable suture). The inferior oblique muscle can also be entrapped by an encircling element.57 In this case, the element is passed behind, or splits, the inferior oblique muscle. When the band is tied in place, the muscle is pulled anteriorly, resulting in a hypotropia and excyclotropia. The hypotropia occurs because the inferior oblique is displaced anteriorly to the

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equator, pulling the front of the eye down. The excyclotropia is caused by the increased tension on the inferior oblique muscle. Torsional diplopia after retinal surgery is not always associated with an entrapped oblique muscle.23 Metz and Norris found two of four patients with torsional diplopia after retinal surgery to have no identiﬁable abnormality of the oblique muscle.72 The complications of oblique muscle entrapments can be diminished by passing the encircling elements anteriorly, just behind the rectus insertions. Extreme posterior passage of the muscle hook may result in inadvertent hooking of an oblique muscle, especially when working on the superior rectus and lateral rectus muscles. The placement of a retinal explant sponge or buckle is often identiﬁed as a primary cause for strabismus after retinal surgery. Transient strabismus after a retinal encircling procedure is frequent, occurring in approximately 20% of cases. In our experience, however, a retinal encircling element by itself rarely causes persistent strabismus. Persistent strabismus after retinal surgery usually results from secondary scarring or a displaced muscle, as stated previously.78 Infrequently, however, a retinal explant may be the primary cause of restriction; this occurs when a large explant is placed directly under a rectus muscle. The explant causes the muscle to deviate from its normal course, thus tightening the muscle. For example, a large retinal sponge placed directly under the medial rectus will cause a tightening of the medial rectus, as the medial rectus courses over the large sponge and produces an esotropia. Low-proﬁle encircling elements, such as 240 bands that indent the sclera, do not interfere with the course of the rectus muscle and, therefore, do not produce strabismus. Foveal ectopia occurs in association with macular pucker, peeling of the epiretinal membrane, and retinal translocation surgery. Acquired foveal ectopia produces an interesting type of strabismus and diplopia. These patients will observe that objects in the central visual ﬁeld appear double, with one image being distorted by metamorphosia. Objects in the peripheral ﬁeld, however, will often be fused, as the peripheral retina may not be involved with the ectopia. Thus, patients who undergo membrane peeling for a macular pucker may experience postoperative diplopia because of foveal ectopia. The image disparities tend to be small with this condition, and prism glasses have been found to be effective in treating this problem.

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Retinal translocation surgery can result in severe torsional diplopia that prisms cannot correct. Instead, oblique muscle surgery is required to treat the problem.38 Extorsion is induced from macular inferior translocation, and intorsion is secondary to superior macular translocation. Extorsion can be corrected by a large Harada–Ito procedure, possibly with an inferior oblique weakening procedure, whereas intorsion can be corrected with a weakening surgery of the superior oblique muscle, perhaps with a tuck of the inferior oblique muscle. Vertical offset of the rectus muscle can also change torsion, but one must consider the risk of anterior segment ischemia in this group of patients.

Glaucoma Explants and Strabismus The incidence of strabismus after glaucoma explant surgery ranges from 10% to 70%, depending on the study.7,90,112 The cause of the strabismus is, for the most part, the large bleb created by the glaucoma explant. Strabismus associated with a large ﬁltering bleb may be caused by the following mechanisms: (1) orbital mass, which displaces the eye (Fig. 10-9); (2) a mass directly under a muscle or tendon; or (3) scarring or adhesions secondary to the surgical dissection during placement of the glaucoma explant. The old Baerveldt implant had been associated with the highest incidence of strabismus; however, modiﬁcations of the Baerveldt implant (fenestrated Baerveldt) have reduced the bleb size and subsequently reduced the incidence of strabismus. Valved implants have also reduced the size of the ﬁltering blebs and have subsequently produced the lowest incidence of strabismus. A large explant in the superior nasal quadrant may cause a pseudo-Brown’s syndrome with restricted elevation in adduction, as the bleb displaces and tightens the superior oblique tendon.7,90 Placement of glaucoma explants should be superotemporal rather than superonasal to avoid the problem of a secondary Brown’s syndrome. The treatment of a bleb-induced strabismus is to reduce the size of the bleb by suturing the bleb wall to the explant so it cannot expand. Additionally, the old explant can be replaced with a newer valved explant. An interesting observation of some patients with strabismus and severe glaucoma is that they do not experience diplopia but, instead, have visual confusion.57 Visual confusion is the simultaneous perception of two different foveal images in a patient

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A

B FIGURE 10-9A,B. Patient with a glaucoma explant in the left superior temporal quadrant. The glaucoma was controlled; however, it produced a large bleb that limited abduction. (A) Patient is looking left, and the left eye shows severe restriction (4) to abduction. (B) Large temporal bleb is causing a mass effect and restricting abduction of the left eye.

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with strabismus. These patients see the superimposed images from each fovea. Patients with end-stage glaucoma have tunnel vision and lose their peripheral visual ﬁeld. If these patients acquire strabismus, they may experience confusion rather than a true diplopia, as they only have central vision and are forced to use the fovea of each eye.

High Myopia and Esotropia (Myopic Strabismus Fixus) High myopia, usually greater than 20 diopters, can be associated with an acquired large-angle esotropia along with limited abduction and a hypotropia9,25,50,63,116; this is a form of acquired strabismus ﬁxus and can be either monocular or binocular. Another term for the high myopia esotropia syndrome is heavy eye syndrome, with hypotropia and limited eye movement.116 Restricted abduction is dramatic, and there is limited elevation of the hypotropic eye. Orbital imaging shows an extremely large globe with a posterior staphyloma that ﬁlls the orbit, a large inferior displacement of the lateral rectus muscle, and a mild nasal displacement of the superior rectus muscle. The cause of the esotropia and hypotropia is a combination of restriction, because of the massive expansion of the posterior globe against a tight medial rectus muscle, and displaced lateral and superior rectus muscles that change the normal vector forces. Displacement of the lateral rectus muscle inferiorly and superior rectus muscles nasally is most likely caused by the massive expansion of the posterior aspect of the globe into the superior temporal quadrant.64 The lateral rectus muscle shows the most displacement, probably due to the laxity of its pulley system. Slippage of the lateral rectus muscle below the globe weakens the abduction vector and pulls the eye down, thus contributing to the esotropia and hypotropia. The nasally displaced superior rectus muscle also contributes to the esotropia and hypotropia by pulling the eye nasally and diminishing the elevation vector force. Treatment is aimed at realigning the lateral rectus muscle and releasing the medial rectus muscle, which is inevitably tight. This author prefers a large recession of the medial rectus muscle, at least 7 to 8 mm on a hang-back suture, and a superior transposition of the lateral rectus muscle with a small resection. The posterior sclera is thin in these cases, and access to the posterior globe is difﬁcult because of the large eye. The hangback suture of the medial rectus allows for a large recession

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without passing a posterior suture. Union of the superior and lateral rectus has also been described.

SPECIFIC TYPES OF PARALYTIC STRABISMUS Sixth Nerve Palsy A persistent, isolated, congenital sixth nerve palsy is extremely rare; however, newborns may have a transient sixth nerve palsy that resolves spontaneously over a few days to a few weeks. A common cause of isolated acquired sixth nerve palsy in early childhood is postviral inﬂammatory neuropathy, which may occur 1 to 3 weeks after a viral illness or immunization or spontaneously without obvious cause. These patients should be followed closely to monitor their improvement and watch for the development of amblyopia. Improvement usually occurs within 6 to 10 weeks. After viral or idiopathic causes, the next most common causes of acquired sixth nerve palsy in children and young adults include closed head trauma and intracranial neoplasms. Neuroimaging is indicated for acquired sixth nerve palsy if the palsy does not improve rapidly or if other neurological signs are present. Other causes of an acquired sixth nerve palsy include Gradenigo’s syndrome (mastoiditis and sixth nerve palsy), meningitis, myasthenia gravis, and cavernous sinus disease. Sixth nerve palsy is typically associated with limited abduction and an esotropia that increases upon gaze to the side of the palsy (Fig. 10-10). On attempted abduction, there is relative lid ﬁssure widening because both the medial and lateral rectus muscles are relaxed on attempted adduction and the posterior orbital pressure proptoses the eye. Remember that, on attempted abduction, the medial rectus muscle is inhibited (Sherrington’s law). Mild sixth nerve paresis may allow relatively good lateral rectus function and show only a trace limitation of abduction. These patients, however, will have a pattern of divergence paresis with an esotropia that is greater in the distance than at near. The divergence paresis pattern should alert the examiner to the possibility of a sixth nerve paresis. Initial therapy of a traumatic or vascular sixth nerve palsy is observation for 6 months while monitoring the patient for spontaneous recovery. Spontaneous recovery of traumatic sixth

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A

B FIGURE 10-10A,B. (A) Photographs of a child with a traumatic right sixth nerve palsy and poor lateral rectus function, evidenced by absent abduction saccades and severe limitation of abduction of the right eye. There is 4 limitation of abduction as the right eye does not go past midline. (B) Results after surgery consisting of a right Hummelsheim transposition and a right medial rectus recession of 6.0 mm. Note the eyes are orthotropic in primary position. There is improved abduction, but abduction remains limited.

nerve palsy is approximately 80% for unilateral cases and 40% for bilateral cases.53 A complete palsy at the initial presentation and bilateral involvement indicate a poor prognosis for recovery.52 During the observation period, alternate monocular occlusion or press-on prisms can be used to eliminate diplopia if a face turn does not allow fusion. To prevent secondary contracture of the medial rectus muscle and increase the chances for recovery, some advocate the use of botulinum injection into the ipsilateral medial rectus muscle.10,74 Botulinum paralyzes the muscle for 3 to 6 months, thus preventing contracture. The hope is that preventing secondary contracture of the medial rectus muscle will increase the chances of recovery without strabismus surgery. The use of botulinum remains controversial, however. Studies comparing botulinum to conservative treatment for the management of nerve palsy have shown no signiﬁcant difference in recovery rates.53,65 Holmes et al., in a prospective multicenter study of acute traumatic sixth nerve palsy or paresis, reported that patients treated either with botulinum or conservatively had similarly high recovery rates.53 It should be noted that, after a botulinum injection into the medial rectus muscle for a complete sixth nerve palsy, both the medial and lateral rectus will be paralyzed, resulting in essentially no horizontal movement of the paretic eye. Therefore, the patient

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should be warned that the paretic eye may have decreased movement after the injection. In addition, the surgeon should be aware that the effects of botulinum can last more than 6 months, and surgery should be delayed until the botulinum has dissipated. After the 6-month observation period, lateral rectus muscle function should be evaluated, as this is critical for determining the surgical plan. Lateral rectus muscle function can be assessed by saccadic velocity testing and the active forced-generation test. If the saccadic velocities are less than 60% of normal or the active forced-generation test is estimated to be half of the normal fellow eye, a vertical rectus muscle transposition procedure is indicated. Transposition procedures act by moving innervated vertical rectus muscles to the lateral rectus insertion to provide lateral force. The lateral force of the transposition does not appropriately activate on attempted abduction but, instead, provides a constant lateral force. Transposition of vertical rectus muscles can involve the full muscle (full-tendon transfer) or the muscle can be split longitudinally and only half the muscle is transferred (partial-tendon transfer). In addition to a transposition, patients with signiﬁcant residual paresis almost always require an ipsilateral medial rectus recession to reduce adduction forces. The vertical rectus muscles provide substantial circulation to the anterior segment. Older adult patients, especially those with arteriosclerotic disease or hyperviscosity syndromes, are at risk for developing anterior segment ischemia after vertical recti transposition, particularly those receiving full-tendon transfers. A partial-tendon transfer procedure should be considered in these patients to maintain anterior circulation and prevent anterior segment ischemia. Modiﬁcations of the Hummelsheim partial-tendon transposition include suturing the transposed vertical muscle to the lateral and resecting a few millimeters of the transposed vertical muscle halves.18,82 An important aspect of the partial-tendon transfer is to fully mobilize the muscle being transferred by splitting the vertical rectus muscles for at least 14 mm posterior to their insertions.135 If carefully performed, a partial-tendon transfer procedure results in long-term good postoperative eye alignment while reducing the risk of anterior segment ischemia. Other options include full-tendon transposition with injection of botulinum toxin to the medial rectus

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TABLE 10-5. Surgical Treatment for Sixth Nerve Palsy. Clinical presentation

Surgery

Excellent lateral rectus function (90%–100%): Ductions trace limitation ET in primary position 2 to 8 PD Diplopia to the side of the palsy Good lateral rectus function (80%–90%) Ductions 1 ET in primary position 10 to 20 PD

Recess contralateral medial rectus 5–6 mm (adjustable suture optional)

Fair lateral rectus function (60%–80%) Ductions 2

ET in primary position 20 to 30 PD Poor lateral rectus function (⬍60%) Ductions 3 to 4

ET in primary position 30 PD

Bilateral medial rectus recessions, but recess the contralateral medial rectus muscle 6 mm and the ipsilateral medial rectus muscle 3–5 mm (adjustable suture advised) Ipsilateral medial rectus recession 6 mm (adjustable suture advised); lateral rectus resection or Wright plication 5 mm and contralateral medial rectus recession 3–5 mm (with optional Faden) Ipsilateral medial rectus recession 6–7 mm (adjustable suture in adults or cooperative children), and vertical rectus partial-tendon transposition to the lateral rectus muscle (either Jensen or Hummelsheim); author prefers modiﬁed Hummelsheim

ET, exotropia.

muscle.102 This treatment, however, may not provide a stable outcome, as an esotropia may recur after 4 to 6 months when the effect of the botulinum dissipates and medial rectus function returns. This author’s recommendations for the surgical treatment of sixth nerve palsy are listed in Table 10-5.

Duane’s Retraction Syndrome The cause of Duane’s retraction syndrome (DRS) has been identiﬁed to be an agenesis of the sixth nerve and nucleus, with the inferior division of the oculomotor nerve (nerve to the medial rectus muscle) splitting to innervate both the medial and lateral rectus muscles.19,31 Because both the medial and lateral rectus muscles are innervated by the nerve to the medial rectus muscle, both muscles ﬁre and contract simultaneously on attempted adduction. This cocontraction of the medial and lateral rectus muscles on adduction gives rise to the term

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Duane’s cocontraction syndrome. Cocontraction of the lateral rectus muscle against the medial rectus muscle on adduction causes globe retraction, producing relative enophthalmos and lid ﬁssure narrowing.94 There are various patterns of innervation that account for the four types of Duane’s syndrome. Figure 10-11 shows a diagram of various patterns of abnormal innervation possible in DRS. Table 10-6 explains the various types of DRS as they correlate to the innervation patterns noted in Figure 10-11. In Duane’s type I, there is agenesis of the sixth nerve and the sixth nerve nucleus, with part of the medial rectus branch of the third nerve going to the lateral rectus muscle. Because most of the medial rectus branch of the third nerve appropriately goes to the medial rectus muscle, the eye will adduct with cocontraction by the aberrantly innervated lateral rectus muscle. This contraction causes lid ﬁssure narrowing; however, because of the absent

A B C D FIGURE 10-11A–D. Diagrammatic representation of misdirection of nerve ﬁbers in Duane’s syndrome. The aberrant nerve pathway is shown in red, and the dotted lines represent nerve hypoplasia or agenesis. (A) type I: poor abduction and good adduction. Agenesis of the sixth nerve and part of the third nerve splits to innervate both the medial and the lateral rectus muscles, but most of the medial rectus nerve goes to the medial rectus muscle so adduction is intact. (B) Type II: poor adduction and good abduction. Sixth nerve is intact and innervates the lateral rectus muscle, but the medial rectus nerve splits to innervate the medial and lateral rectus muscles. There is poor adduction because the lateral rectus contracts against the medial rectus muscle. (C) Type III: poor adduction and poor abduction. Agenesis of the sixth nerve and part of the third nerve splits to innervate both the medial and the lateral rectus muscles. The split is equal so the eye does not move in or out. (D) Synergistic divergence and paradoxical abduction on attempted adduction. Agenesis of the sixth nerve and part of the third nerve splits to innervate both the medial and the lateral rectus muscles, but most of the medial rectus innervation goes to the lateral rectus muscle. When the eye attempts to adduct, it abducts because the medial rectus nerve innervates the lateral rectus muscle.

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TABLE 10-6. Classiﬁcation of Duane’s Syndrome. Type I Duane’s: most common Poor abduction and good adduction. The medial rectus muscle receives most of the medial rectus nerve innervation and the lateral rectus receives minimal innervation from the medial rectus nerve, with agenesis of the sixth nerve. Because the medial rectus receives most of the innervation, the Duane’s eye is usually ﬁxed in an adducted position with an esotropia in primary position, and there is a compensatory face turn in the direction of the Duane’s eye (i.e., left face turn for a left Duane’s type I). Type II Duane’s: least common, extremely rare Poor adduction and good abduction. EMG recordings show the lateral rectus muscle to contract appropriately on abduction, but it also contracts paradoxically on adduction; this probably represents a partial innervation of the lateral muscle by the sixth nerve nucleus (as purposeful abduction is present), plus splitting of the medial rectus nerve to innervate the medial and lateral rectus muscles. Type III Duane’s: second most common Poor adduction and poor abduction (the eye has little horizontal movement). Equal innervation of the medial and lateral rectus muscles by the medial rectus nerve, with congenital absence of the sixth nerve. Because the medial and lateral forces are similar, the eye will rest in approximately primary position and there will be no signiﬁcant face turn. In some cases, an exotropia is present in primary position because the lateral rectus receives slightly more innervation than the medial rectus muscle; this causes a face turn away from the Duane’s eye. Synergistic divergence: extremely rare Paradoxical abduction on attempted adduction and poor abduction. Little or no innervation of the lateral rectus by the sixth nerve. Most of the medial rectus nerve goes to the lateral rectus muscle. On attempted adduction, the lateral rectus is stimulated by the medial rectus nerve and the eye paradoxically abducts.

sixth nerve, there is no abduction (Fig. 10-12). If the medial rectus nerve equally innervates the medial and lateral rectus muscles, then the cocontraction of the lateral rectus muscle will equal the appropriate contraction of the medial rectus muscle, and the eye will have limited adduction in addition to limited abduction because of the sixth nerve agenesis. This pattern of poor adduction and abduction is typical of Duane’s type III (Fig. 10-13). In the rare Duane’s type II syndrome, abduction is intact but is limited because part of the sixth nerve innervates the lateral rectus muscle and part of the medial rectus nerve innervates the lateral rectus muscle. Another rare form of Duane’s syndrome is synergistic divergence. In this syndrome, most of the third nerve that should innervate the medial rectus muscle aberrantly innervates the lateral rectus muscle, causing the Duane’s eye to paradoxically abduct on attempted adduction.124

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FIGURE 10-12. Duane’s syndrome type I, left eye. Inset shows a face turn to the left, eyes shifted left to maintain binocular fusion. Composite shows limited abduction in left eye, esotropia in primary position, and lid ﬁssure narrowing of left eye on adduction. Note that in primary position the Duane’s eye (left eye) is ﬁxing so there is a secondary esodeviation of the right eye. A positive Brückner reﬂex is seen from the esotropic right eye.

FIGURE 10-13. Composite photograph of a child with Duane’s syndrome type III, right eye. There is almost no adduction or abduction in the right eye, and the right eye is ﬁxed in the abducted position. Lid ﬁssure narrowing of right eye occurs on attempted adduction. In primary position, there is an exotropia and this patient adopts a compensatory face turn to the left to keep the eyes aligned in right gaze.

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A patient with right synergistic divergence will diverge and have a large exotropia on attempted leftgaze.124 Duane’s syndrome is present at birth and is usually unilateral, but it can be bilateral.54 If there is a deviation in primary position, patients with DRS will adopt a compensatory face turn to obtain binocular fusion. The face turn is determined by the resting position of the Duane’s eye. If the medial and lateral rectus muscles receive comparable innervation from the split oculomotor nerve and the eye is centered in primary position, there will be no signiﬁcant face turn (Duane’s type III). If, however, the medial rectus muscle receives most of the innervation from the oculomotor nerve, then the affected eye will rest in adduction and the patient will have an esotropic DRS with a face turn toward the side of the affected eye (Duane’s type I). Less commonly, the lateral rectus will receive most of the innervation from the oculomotor nerve. In these cases, the Duane’s eye will be abducted, causing an exotropia (XT) in primary position and a face turn toward the opposite side of the Duane’s eye (Duane’s type III with an XT).94 Duane’s syndrome may be associated with an upshoot or a downshoot on attempted adduction, which may resemble inferior oblique and superior oblique overaction (Fig. 10-14). Studies utilizing EMGs have identiﬁed a variety of aberrant innervation patterns that explain the vertical movements on adduction.55,107,115 In some cases, the upshoot and downshoot are caused by strong, inappropriate ﬁring of the lateral rectus muscle on adduction. This leash effect pulls the eye up or down, as the eye rotates slightly up or down past the horizontal plane. In other cases, the vertical recti are aberrantly innervated by part of the medial rectus nerve, so the vertical muscle ﬁres on adduction. Other oculomotor misdirection syndromes are associated with Duane’s syndrome, such as Marcus Gunn jaw-winking. Duane’s syndrome is associated with numerous systemic syndromes including Goldenhar’s syndrome, Klippel–Feil syndrome, maternal thalidomide ingestion, fetal alcohol syndrome, and oculocutaneous albinism.31

SURGICAL EVALUATION Indications for surgery in DRS include (1) signiﬁcant misalignment of the eyes in primary position, (2) noticeable abnormal head position, (3) narrowing of palpebral ﬁssure due to retrac-

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A

B FIGURE 10-14A,B. Photographs of an upshoot (A) and downshoot (B), right eye, occurring on attempted adduction associated with Duane’s syndrome of right eye.

tion, and (4) signiﬁcant upshoot or downshoot. Usually, surgery is electively performed around age 3 to 8 years, as these patients have excellent fusion and the condition is stable. Rarely will a DRS patient have amblyopia and, when present, it is almost always associated with anisometropia. Amblyopia should be

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the ﬁrst priority in these unusual cases. In general, muscle resections should be avoided in DRS, because resections can make the cocontraction and lid ﬁssure narrowing worse.

SURGERY FOR DRS TYPE I IPSILATERAL FACE TURN

WITH

ESOTROPIA

AND

In cases with esotropia and Duane’s type I, the Duane’s eye is in an adducted position and there is a face turn toward the Duane’s eye. The medial rectus muscle is usually contracted and tight. The simplest, most effective treatment for Duane’s type I with esotropia is an ipsilateral medial rectus recession (between 5.0 and 7 mm). In adult patients, place the medial rectus muscle on an adjustable suture and adjust to a 5° to 10° overcorrection so there is a small exotropia in primary position; this results in stable long-term correction of the face turn. Remember, the lateral rectus muscle is not denervated, as in the case of a sixth nerve palsy, but has innervation provided by part of the medial rectus nerve. This tonic innervation provides stabilizing abduction force, so a muscle transposition procedure is not required. Some have advocated a transposition of the vertical rectus muscles laterally for DRS and esotropia. This procedure is more invasive and has the risk of producing anterior segment ischemia. The transposition procedure also has a risk of inducing a vertical deviation in approximately 15% of patients. This author prefers the simple and effective ipsilateral medial rectus recession for Duane’s type I with esotropia.

SURGERY FOR DRS TYPE III WITH EXOTROPIA CONTRALATERAL FACE TURN

AND

In a patient with Duane’s and exotropia, it is almost always a Duane’s type III. The eye is resting in abduction, and the face turn is away from the Duane’s eye. There is usually a tight lateral rectus muscle, and these patients require an ipsilateral lateral rectus recession. If there is an upshoot or downshoot associated with the Duane’s type III, then consider a Y-split procedure with the lateral rectus recession.

TREATMENT

OF

GLOBE RETRACTION

Globe retraction can be diminished by recessing both the ipsilateral medial rectus and lateral rectus muscles. In patients with esotropic DRS and severe globe retraction, add a lateral rectus recession, but recess the medial rectus muscle more than the lateral rectus to compensate for the esotropia. In exotropic DRS,

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recess the lateral rectus more than the medial rectus muscle or, for a large exotropia, recess only the lateral rectus muscle (large recession). For orthotropic DRS without a face turn, recess the medial and lateral rectus muscles the same amount.

TREATMENT

OF

UPSHOOT

AND

DOWNSHOOT

Two approaches to reduce upshoot and downshoot associated with DRS include these: 1. Y-splitting with recession of the lateral rectus muscle 2. Posterior ﬁxation suture (Faden) of the lateral rectus and appropriate recession of horizontal recti The Y-splitting procedure of the lateral rectus muscle works by placing some of the lateral rectus muscle above and below the horizontal midline, thus preventing an upshoot or downshoot when the eye is in adduction.95,100 By combining a recession of the lateral rectus muscle with the Y-split, one can treat both an exotropia Duane’s type III with an upshoot and downshoot. In patients with orthotropic DRS and a severe upshoot and downshoot, recess the ipsilateral medial rectus muscle along with a recession and Y-split of the ipsilateral lateral rectus muscle. The posterior ﬁxation suture acts to stop slippage of the lateral rectus muscle when the eye rotates up or down, and a concurrent recession reduces cocontraction. The authors have found the Ysplitting procedure is more effective than the posterior ﬁxation suture.

Fourth Nerve Palsy (Superior Oblique Palsy) See Chapter 9.

Third Nerve Palsy Third nerve palsy involves all the extraocular muscles except the lateral rectus and the superior oblique. The strabismus is characterized by the eye being “down and out” with a small hypotropia and a large exotropia (Fig. 10-15). There is limited depression, elevation, and adduction, along with preservation of abduction (intact innervation lateral rectus muscle) and intorsion seen on attempted eye movement down and in (intact innervation superior oblique muscle). Ptosis, pupillary dilatation, and hypoaccommodation are also present in a complete third nerve palsy. A congenital third nerve paresis is often

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FIGURE 10-15. Photograph of a left third nerve palsy; there is a left ptosis and the left eye is “down and out” (left exotropia and hypotropia).

partial, without ptosis, with variable amounts of limited elevation, depression, and adduction, with pupillary sparing, and may show oculomotor synkinesis. The two most common causes of pediatric third nerve palsy are idiopathic congenital onset and head trauma. Other causes include migraine, an association with a viral syndrome, an intracranial tumor, or, rarely, a posterior communicating aneurysm.14,62,105 Nontraumatic acquired third nerve palsy cases must undergo a full workup with neuroimaging.62

TREATMENT The treatment of complete third nerve palsy is extremely difﬁcult because there are no vertical muscle forces to move nasally, as all the vertical recti are paretic. Superior oblique tendon transfer to the medial rectus insertion has been suggested as a way of providing medial forces.104 This procedure, however, does not increase adduction as it only creates a leash and limits depression of the eye, resulting in a large hypertropia in downgaze. An ipsilateral superior oblique tenotomy, with ipsilateral recession of the lateral rectus and a large resection of medial rectus, is probably the procedure most often used for a third nerve paresis with an exotropia and hypotropia and some medial rectus function. In cases where this procedure has failed to correct the

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exotropia, this author has split the lateral rectus and transposed the halves to the nasal border of the superior and inferior rectus muscles. This procedure has worked in centering the eye; however, horizontal excursions are minimal. In addition to the difﬁculty in treating the strabismus, patients with a third nerve palsy and ptosis with poor or absent levator function, are at risk for developing corneal exposure if the ptosis is repaired. Ptosis should be managed with a silicone frontalis sling procedure, aiming for intentional undercorrection of the lid position if there is a poor Bell’s phenomenon. The silicone sling procedure has an advantage of being reversible if corneal exposure becomes a problem. Patients should be warned about the risk of corneal exposure and that their diplopia may be worse after lifting the eyelid, as this removes the occlusion. Many wise patients and physicians opt for leaving the ptosis alone if associated with a poor superior rectus muscle function evidenced by a poor Bell’s phenomenon.

Inferior Oblique Paresis See Chapter 9.

Möbius Syndrome Möbius syndrome is characterized by a combination of facial palsy, sixth nerve palsy, partial third nerve palsy, and distal limb abnormalities such as syndactyly, club foot, or even amputation defects.23 There is some degree of intellectual impairment in 75% of patients.23,131 The Möbius infant typically presents with esotropia, limited abduction, lack of facial expression, and difﬁculty feeding caused by a poor sucking reﬂex. Craniofacial anomalies can occur and include micrognathia, tongue abnormalities, and facial or oral clefts. Ocular motility abnormalities include limited abduction in more than 90% of cases and limited adduction in 65% of cases.23,66,86 Some patients have globe retraction on adduction and failure to abduct, typical of Duane’s syndrome. The inheritance pattern of Möbius syndrome is usually sporadic, and there is great variability of ﬁndings,44 suggesting that the syndrome represents a heterogeneous group of neuromuscular disorders.87 Prenatal exposure to misoprostol, the abortion-inducing drug, has been implicated as a risk factor.23,41,120 Treatment of the strabismus is tailored to the individual situation. Patients with a large esotropia, tight medial rectus

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muscles, and poor abduction are probably best treated with large bilateral medial rectus recessions similar to the treatment of a patient with congenital ﬁbrosis syndrome.

Sinus Surgery and Medial Rectus Muscle Injury Endoscopic sinus surgery can result in severe damage to the medial rectus muscle and even visual loss.31,69,98 This damage occurs when the thin ethmoid bone is violated during endoscopic sinus surgery and the medial rectus muscle is traumatized. In most cases, part of the medial rectus muscle is removed, often in the area of the neuromuscular junction (two-thirds of the way back from the insertion or approximately 25 mm posterior to the insertion). On MRI, the medial rectus may be seen to be myectomized and pulled into the ethmoid sinus (Fig. 10-16). The inferior rectus and inferior oblique muscles can also be traumatized, but this is less common.98 Treatment of the adduction deﬁcit and exotropia depends on the extent of the damage to the medial rectus muscle and the state of the innervation.119 Unfortunately, in most cases, there is poor medial rectus muscle function secondary to neuromuscular junction injury or a posterior myectomy. If medial rectus muscle function is poor, a partial-tendon transfer of the vertical rectus muscle to the medial rectus insertion (Hummelsheim) or a procedure to create a nasal tether to pull the eye to midline is indicated.6 Standard exploration and muscle retrieval techniques (used for locating lost muscles) do not work if the injury involves the neuromuscular junction or if a posterior myectomy was performed.

Aplasia of Extraocular Muscles Although virtually all extraocular muscles have been described as being congenitally absent, the inferior rectus is most commonly affected.13,70,101 The condition is often associated with craniofacial dysostosis, anencephaly, or other congenital head anomalies.8,22,42,88,113 Aplasia of the inferior rectus, superior rectus, and superior oblique muscles can occur in otherwise healthy children without craniofacial abnormalities.27,58,67 Figure 10-17 depicts a case in which this author surgically explored to ﬁnd aplasia of the right inferior rectus and hypoplasia of the left inferior rectus muscle. This child was healthy and presented with a right hypertropia and bilateral limited depression, right eye more than left eye. An absent rectus muscle is managed by

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A

B FIGURE 10-16A–B. Photographs of patient with right medial rectus injury associated with sinus surgery. (A) Rightgaze, full motility. (B) Primary position with right exotropia.

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C

D FIGURE 10-16C–D. (C) Leftgaze, showing no signiﬁcant adduction of right eye. This patient had no adduction saccade. (D) MRI shows the posterior aspect of the right medial rectus has been myectomized, and the posterior cut end of the muscle is entrapped in the ethmoid sinus.

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A

B FIGURE 10-17A,B. Photographs of bilateral asymmetrical inferior rectus muscle hypoplasia (surgeon’s view) at the time of surgery. Patient presented with a right hypertropia and severe limitation of depression, rightgaze. (A) The left eye has an underdeveloped inferior rectus muscle. (B) The right inferior rectus muscle shows only the anterior ciliary vessels, but there is no inferior rectus muscle (i.e., aplasia of the inferior rectus muscle).

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a Hummelsheim-type transposition procedure to substitute for the absent muscle.

Craniosynostosis Causes for strabismus associated with craniosynostosis include divergent orbits, displaced extraocular muscles agenesis of extraocular muscles, and extorsion of the orbits.22,42,88,113 A common pattern of strabismus seen in patients with a variety of craniosynostosis syndromes is exotropia with apparent severe bilateral inferior oblique overaction, superior oblique underaction, and a large V-pattern (Fig. 10-18). The possible causes for the inferior oblique overaction and V-pattern can be an absence of the superior oblique tendon or extorted orbits.9 Extorted orbits shift the medial rectus up and the lateral rectus down so the medial rectus pulls the adducting eye up and the lateral rectus pulls the abducting eye down, which simulates inferior oblique overaction. Likewise, the inferior rectus muscle are displaced nasally and the superior rectus muscle temporally so that in downgaze the eyes converge and in upgaze they diverge.20

FIGURE 10-18. Photograph of patient with Pfeiffer syndrome. Motility exam showed an exotropia, inferior oblique overaction, superior oblique underaction, and V-pattern. Note the extreme underaction of the right superior oblique muscle as the patient looks down and to the left.

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DISSOCIATED VERTICAL DEVIATION AND DISSOCIATED HORIZONTAL DEVIATION Dissociated vertical deviation (DVD) is the tendency for an eye to elevate, abduct, and extort, when binocularity is suspended by occlusion or the patient spontaneously dissociates (often when fatigued). DVD is almost always bilateral, but asymmetrical cases may appear to be unilateral. Prolonged occlusion of the eye that appears not to have DVD, however, will almost always disclose a latent DVD. Note that, with a true hypertropia, there is a corresponding hypotropia of the fellow eye and, on alternate cover testing when the hypertropic eye moves down into primary position, the fellow eye also moves down to become hypotropic. Thus, a true hypertropia is consistent with Hering’s law of yoke muscles. In contrast, DVD violates Hering’s law of yoke muscles because covering the right eye makes the right eye drift up, and covering the left eye makes the left eye drift up with no corresponding hypotropia of the fellow eye (Fig. 10-19). One can think of DVD as two individual hypertropias that are dissociated, thus the term, dissociated vertical deviation. DVD increases on head tilt: head tilt to the right increases a right DVD and head tilt to the left increases a left DVD. DVD occurs when normal binocular visual development is disrupted and is associated with congenital esotropia, congenital exotropia,11 congenital media opacities (e.g., monocular congenital cataracts), and even unilateral optic nerve hypoplasia. Rarely, this author has seen patients with primary DVD; that is, no horizontal strabismus, and no history of previous strabismus surgery (Fig. 10-19). These patients usually have some degree of stereoacuity, sometimes high-grade stereoacuity. On version testing, DVD can mimic inferior oblique overaction because the vision of the adducting eye is blocked by the bridge of the nose; this dissociates the eyes, causing the DVD of the adducting eye to be manifest. The two can be distinguished, however, as DVD has no true hypotropia of the opposite eye, and the hyperdeviation is the same in abduction as in adduction. With inferior oblique overaction, there is a hypotropia of the opposite eye and the deviation increases as the eye moves into adduction. DVD and inferior oblique overaction often coexist with congenital esotropia.127 The cause of dissociated vertical deviation is unknown. Guyton hypothesized that abnormal binocular development causes unbalanced input to the vestibular system, resulting in

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A

B FIGURE 10-19A,B. Photographs of bilateral dissociated vertical deviation (DVD). Patient has primary DVD with excellent stereoacuity and has never had strabismus surgery. (A) The left eye is covered to manifest the left DVD. (B) The right eye is covered and discloses a right DVD. Note that the eye behind the cover is not only elevated but is also slightly exodeviated.

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latent nystagmus with a cyclovertical movement. Cycloversion/ vertical vergence is invoked to damp the cyclovertical nystagmus (a cyclovertical “nystagmus blockage” phenomenon), aiding vision in the ﬁxing eye. Unfortunately, this mechanism also produces unavoidable and undesirable elevation and extorsion of the fellow eye that results in DVD.45 This author has a theory about the neurophysiological basis for DVD. It is interesting that DVD is associated with disruption of early binocular visual development. The interstitial nucleus of Cajal is a brainstem nucleus that regulates cyclovertical movements. The interstitial nucleus of Cajal receives inhibitory input from binocular cells in the occipital cortex, and these inhibitory pathways act to control this nucleus. Lesions around the interstitial nucleus of Cajal that interrupt the binocular inhibitory input result in nucleus disinhibition, which is clinically manifested as seesaw nystagmus. Seesaw nystagmus is a dissociated cyclovertical/horizontal nystagmus. When seesaw nystagmus occurs in infancy, it can look quite similar to DVD. Infantile strabismus or a dense monocular congenital cataract disrupts binocular visual development and reduces binocular cortical cells. Perhaps the lack of binocular cortical cells associated with congenital strabismus or a unilateral blurred retinal image in infancy, results in reduced binocular inhibitory input to the interstitial nucleus of Cajal or similar cyclovertical brainstem nuclei. Reduced binocular inhibitory input would cause disinhibition of these cyclovertical nuclei, giving rise to what we see clinically as DVD. If early surgery for infantile esotropia improves binocularity, then children who have had early surgery should have less DVD. Recent reports on the incidence of DVD in children who have had early surgery for infantile esotropia, however, remain unchanged from reports 30 years previous.81,136 Even though the incidence may be the same, the severity of DVD seems to have diminished over the past few decades. It is this author’s opinion, along with the observations of senior expert strabismologists, that the incidence of severe DVD requiring surgery has decreased. Performing surgery for a large, cosmetically obvious DVD in the 1970s and early 1980s was commonplace. As a resident in ophthalmology, this author remembers operating every month on several DVD patients. Over the past several years, there have only been a few cases requiring surgery, and usually on older adults with DVD. The author’s visits to countries where surgeons continue to operate late, after 2 years of age, have disclosed that a very high prevalence of big, surgically

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signiﬁcant DVD persists. Perhaps, with the advent of early intervention of infantile esotropia in this country, our children with infantile esotropia have been able to establish better binocular fusion, thus reducing the severity, but not the incidence, of the DVD. In this author’s report on very early surgery for congenital esotropia (surgery between 13 and 19 weeks of age), four of seven patients had DVD on last examination (2–8 years; mean, 4 years).136 This DVD, however, was very small and could only be demonstrated by prolonged cover testing. None of the patients required DVD surgery, although one had surgery for inferior oblique overaction. M cell afferent pathway development is responsible for motor fusion and control. Because M cell development starts very early, around 6 weeks to 2 months of age, perhaps our “very early surgery” is not early enough to establish strong motor fusion and eliminate DVD.137 The treatment of DVD is surgical, and surgery is indicated if the DVD exists to the point that it becomes a cosmetic problem. DVD is most often bilateral, and bilateral surgery is usually performed. An exception is with amblyopia, where surgery is performed only on the amblyopic eye. With amblyopia of 2 lines or more, the patient will always ﬁxate with the sound eye, and the sound eye will not manifest the DVD. Most consider superior rectus recessions as the treatment choice for pure DVD without inferior oblique overaction. If DVD and inferior oblique overaction coexist, then an anterior transposition of the inferior oblique is indicated, as this will address both problems with one procedure.12,43,93,121 Strabismus surgery rarely, if ever, cures DVD. Dissociated horizontal deviation (DHD), which may be unilateral or bilateral, is a subtype of DVD that often occurs in patients who have had previous strabismus surgery for congenital esotropia.129 This is a dissociated condition like DVD, but the exocomponent of DVD is exaggerated. Cover/uncover testing may show no shift or a small esotropia, but prolonged occlusion produces an exodeviation. Think of DHD when examining patients with a small residual esotropia, who also have a dissociated exodeviation. The treatment of DHD is recession of the ipsilateral lateral rectus muscle.128

Torticollis and Face Turns This section covers the approach to patients who present with an abnormal head posture. Abnormal head posturing includes torticollis (head tilt), chin elevation and depression, and face

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turn. These forms of head posturing can occur independently or in combination, as a patient with a superior oblique palsy will often have both a head tilt and a face turn. Torticollis can be secondary to a musculoskeletal abnormality of the neck or to an ocular problem compensated by head posturing. A simple initial test to determine the cause is to ask the patients to close their eyes and observe for several seconds to see if the head posturing spontaneously improves. If the face turn improves when the eyes are closed, this suggests an ocular cause. Next, passively move the patient’s head from side to side with the patient’s eyes closed. If the range of motion of the head and neck is normal, this veriﬁes that the head posturing is an ocular torticollis; however, a stiff neck indicates a musculoskeletal problem. By far the most common ocular causes of abnormal head posturing are nystagmus with a null point and incomitant strabismus with compensatory head posturing to allow fusion. A face turn is often identiﬁed by observing the patient’s head posture. A better way to evaluate the presence of a face turn is to observe the position of the eyes. Normal patients with straight eyes and no face turn will have both eyes centered within the palpebral ﬁssures. If a face turn is present, there will be a gaze preference with the eyes constantly shifted opposite to the face turn. For example, a face turn to the right is associated with eyes shifted to the left (Fig. 10-20), and a chin elevation will have the eyes shifted down. When examining a patient for a face turn, ﬁrst observe the position of the eyes and the presence of a gaze preference. Next, turn or tilt the head opposite to the compensatory position to place the eyes into the nonpreferred ﬁeld of gaze. If there is a face turn to the right, turn the head to the left; if there is a head tilt to the right, tilt the head to the left. While the head is held opposite to the compensatory position, observe for nystagmus or strabismus. If nystagmus occurs or increases with a forced face turn to the opposite side, then a compensatory face turn is present to keep the eyes in the area of the null point. If strabismus is produced by forced head tilt, or turns the eye in with a previously fusing patient, then the compensatory head posturing is adopted to maintain fusion, keeping the eyes in the ﬁeld of gaze where the eyes are aligned. In addition to face turns and head tilts, chin elevations or depressions can be compensatory for nystagmus or strabismus, and chin elevations compensate for ptosis. The degree of face turn can be measured by using an orthopedic goniometer placed on the head. Any protractor will work

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FIGURE 10-20. Photograph of ocular torticollis in a patient with nystagmus. Patient has a face turn to the right to place the eyes at the null point in leftgaze. The best way to identify a face turn is to evaluate the position of the eyes. If there is a strong gaze preference for an eccentric gaze position, then consider the possibility of a compensatory face turn.

as the line of sight is compared to the direction of the face, with the nose as the pointer.77 An alternative method for measuring face turn associated with Duane’s syndrome or unilateral limited eye movement is to place a prism over the eye with limited rotation, with the apex pointing toward the direction of the deviated eye. The prism is progressively increased until the face turn is corrected. The amount of prism required to neutralize the face turn is recorded in prism diopters. Prism diopters can be converted to degrees by dividing by 2. Prism correction of head posturing can also be used to measure face turns associated with nystagmus.

Incomitant Strabismus Causing Compensatory Head Posturing Head posturing compensates for incomitant strabismus by placing the eyes in a ﬁeld of gaze where the eyes are best aligned to achieve binocular fusion. For example, a patient with a left sixth nerve palsy will have a large esotropia in leftgaze and straight eyes in rightgaze. These patients will adopt a face turn to the left to keep their eyes aligned in rightgaze. An incomitant

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strabismus where the eyes are aligned in an eccentric ﬁeld of gaze can cause an abnormal head posture; this includes cranial nerve palsies, restrictive strabismus, A- or V-patterns, and primary oblique dysfunction. For example, patients with fusion and an A-pattern exotropia or V-pattern esotropia will show a chin depression (eyes straighter in upgaze), whereas an A-pattern esotropia or V-pattern exotropia will show a chin elevation (eyes straighter in downgaze). The treatment of an abnormal head posture caused by incomitant strabismus is simply to correct the strabismus in primary position and provide a large ﬁeld of single binocular vision. If the ﬁxing eye has limited ductions, then move the eye with limited movements to primary position, and the normal eye will follow.

Nystagmus Causing Compensatory Head Posturing A compensatory head posture can stabilize nystagmus by placing the eyes at the null point. If the null point is to the right, the patient will shift the eyes to the right and have a face turn to the left. Head posturing associated with nystagmus can take the form of a face turn, chin elevation or depression, or a head tilt. A compensatory face turn associated with congenital nystagmus can be treated using eye muscle surgery to move the eye position from the null point to primary position.77 The general surgical principles for correcting a face turn are as follows5: 1. Kestenbaum–Anderson–Parks (Kestenbaum) procedure: With a compensatory face turn to the right, the eyes will be shifted to the left. Therefore, to correct the face turn, move the eyes to the right into primary position (Fig. 10-21), which is done by moving the right eye out (right medial rectus recession–right lateral rectus resection) and moving the left eye in (left lateral rectus recession and a left medial rectus resection). The amount of surgery for a speciﬁc amount of face turn is listed in Table 10-7. Note, Parks Poker Straight 5-6-7-8 (medial recession 5 mm, medial resection 6 mm, lateral recession 7 mm, and lateral resection 8 mm) is a way of remembering the amount of surgery for a small face turn. In most cases, however, larger amounts of surgery are needed.77 Large recessions and resections are needed for a face turn associated with nystagmus. Postoperative

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FIGURE 10-21. Drawing showing how to correct a face turn to the right associated with nystagmus using the Kestenbaum procedure. The view is looking down on a face turn to the right with eyes in leftgaze at the null point. Surgically correct the face turn by simply moving the eyes into primary position. The arrows in the diagram indicate moving the eyes to the right to place the eyes in primary position. The left eye is shifted nasally (recess lateral rectus muscle and resect the medial rectus muscle) and the right eye moved temporally (recess medial rectus muscle and resect the lateral rectus muscle) to correct the face turn.

TABLE 16-7. Kestenbaum Procedure for Nystagmus with a Face Turn to the Right (Eyes Shifted Right). Left eye Face turn (degrees)

Right eye

Recess lateral rectus (mm)

Resect medial rectus (mm)

Recess medial rectus (mm)

Resect lateral rectus (mm)

7 9 10 11

6 8 8.5 9.5

5 6.5 7 8

8 10 11 12.5

20 30 45 50 See Figures 10-20, 10-21.

Source: Modiﬁed from Refs. 5, 135, permission.

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limitation of ocular movements is to be expected, deemed to be an acceptable trade-off. 2. Vertical head posturing: Chin depression (eyes up) is treated with large bilateral superior rectus recessions (8–9 mm) and inferior rectus resections (6–7 mm). For large chin depressions, this can be combined or performed in stages, the superior rectus recessions ﬁrst, then inferior rectus resections later if necessary. Chin elevations (eyes down) can be treated similarly by recessing the inferior rectus muscles (7–8 mm) and resecting the superior rectus muscles (6–7 mm).99 Surgical therapy should be based on the greatest amount of abnormal head posture measured at distance and near. For example, if the face turn is obvious at distance and not at near, full correction directed at the face turn in the distance should be undertaken. When strabismus coexists with nystagmus, the head posture can be corrected by moving the ﬁxing eye to primary position. Then adjust the fellow eye to compensate for the residual strabismus. Compensatory head tilts are also associated with nystagmus, which can be corrected by rotating the eyes back to primary position. A head tilt to the right can be treated by surgically extorting the right eye and intorting the left eye.122

SURGICAL TREATMENT OF NYSTAGMUS: NO FACE TURN Although the Kestenbaum–Anderson–Parks procedure is directed toward eliminating the abnormal horizontal face turn associated with nystagmus, another approach has been described to damp nystagmus in patients without a face turn. Simultaneous retroequatorial recessions of all four horizontal rectus muscles have been reported to decrease the amplitude of nystagmus and improve visual acuity.30,36,97 The precise mechanism responsible for damping the nystagmus is not known, and the long-term effect remains unknown. Vision improves only in cases of motor nystagmus, not in patients with sensory nystagmus who have an abnormal afferent pathway.

Additional Causes of Ocular Torticollis Less common mechanisms for head posturing do exist. Rarely, a patient with diplopia adopts a head posture that induces maximal image separation rather than fusion, thus making suppression of the diplopic image easier. Other reasons for abnor-

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mal head posturing include compensation for visual ﬁeld defects, restriction of the good eye in monocular patients, manifest latent nystagmus with a face turn to keep the ﬁxing eye in adduction, ptosis with chin elevation, tilting for monocular torsion, and cosmetic reasons. Other causes include asymmetrical dissociated vertical deviation, refractive error in which the patient adopts a face turn presumably to partially block the pupil, inducing a pinhole effect that provides better visual acuity.

References 1. Amemiya T, Yoshida H, Harayama K, et al. Long-term results of retinal detachment surgery. Ophthalmologica 1978;177:64–69. 2. Anderson RL, Baumgartner SA. Strabismus and ptosis. Arch Ophthalmol 1980;98:1062–1067. 3. Appleton RE, Chitayat D, Jan JE, Kennedy R, Hall JG. Joubert’s syndrome associated with congenital ocular ﬁbrosis and histidinemia. Arch Neurol 1989;46(5):579–582. 4. Apt L, Axelrod RN. Generalized ﬁbrosis of the extraocular muscles. Am J Ophthalmol 1978;85(6):822–829. 5. Archer SM. Strabismus surgery planning. In: Del Monte MA, Archer SM (eds) Atlas of pediatric ophthalmology and strabismus surgery. New York: Churchill Livingstone, 1993:14. 6. Awad AH, Shin GS, Rosenbaum AL, Goldberg RL. Autogenous fascia augmentation of a partially extirpated muscle with a subperiosteal medial orbitotomy approach. J AAPOS. 1997;1(3):138–142. 7. Ball SF, Ellis GS, Herrington RG, Liang K. Brown’s superior oblique tendon syndrome after Baerveldt glaucoma implant. Arch Ophthalmol 1991;110:1368. 8. Barnes RJ. Anencephaly with absence of superior oblique tendon. Surv Ophthalmol 1972;16:371–374. 9. Bagshaw J. The ‘heavy eye’ phenomenon. A preliminary report. Br J Ophthalmol 1966;23:73–78. 10. Biglan AW, et al. Management of strabismus with botulinum A toxin. Ophthalmology 1989;96:935–943. 11. Biglan AW, Davis JS, Cheng KP, Pettapiece MC. Infantile exotropia. J Pediatr Ophthalmol Strabismus 1996;33(2):79–84. 12. Black BC. Results of anterior transposition of the inferior oblique muscle in incomitant dissociated vertical deviation. JAAPOS 1997; 1(2):83–87. 13. Brady AP, Stack JP, O’Keeffe M. Congenital absence of extraocular muscles: MR demonstration. J Comput Assist Tomogr 1992;16(3): 490–491. 14. Branley MG, Wright KW, Borchert MS. Third nerve palsy due to cerebral artery aneurysm in a child. Aust NZ J Ophthalmol 1992;20: 137–140.

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15. Bremer DL, Rogers GL, Quick LD. Primary-position hypotropia after anterior transposition of the inferior oblique. Arch Ophthalmol 1986;104:229–232. 16. Brodsky MC. Hereditary external ophthalmoplegia synergistic divergence, jaw winking, and oculocutaneous hypopigmentation: a congenital ﬁbrosis syndrome caused by deﬁcient innervation to extraocular muscles. Ophthalmology 1998;105(4):717–725. 17. Brooks SE, Ribeiro GB, Archer SM, Elner VM, Del Monte MA. Fat adherence syndrome treated with intraoperative mitomycin-C: a rabbit model. J Pediatr Ophthalmol Strabismus 1996;33(1):21–27. 18. Brooks SE, Olitsky SE, de Ribeiro G. Augmented Hummelsheim procedure for paralytic strabismus. J Pediatr Ophthalmol Strabismus 2000;37(4):189–195; quiz 226–227. 19. Capo H, Guyton DL. Ipsilateral hypermetropia after cataract surgery. Ophthalmology 1996;103:721–730. 20. Cheng H, Burdon MA, Shun-Shin GA, Czypionka S. Dissociated eye movements in craniosynostosis: a hypothesis revisited. Br J Ophthalmol 1993;77:563–568. 21. Coats DK, Paysse EA, Plager DA, Wallace DK. Early strabismus surgery for thyroid ophthalmopathy. Ophthalmology 1999;106(2): 324–329. 22. Coats DK, Ou R. Anomalous medial rectus muscle insertion in a child with craniosynostosis. Binoc Vis Strabismus Q 2001;16(2):119– 120. 23. Cronenberger MF, de Castro Moreira JB, Brunoni D, et al. Ocular and clinical manifestations of Möbius’ syndrome. J Pediatr Ophthalmol Strabismus 2001;38(3):156–162. 24. Cruz OA, Davitt BV. Bilateral inferior rectus muscle recession for correction of hypotropia in dysthyroid ophthalmopathy. JAAPOS 1999;3(3):157–159. 25. Demer JL, von Noorden GK. High myopia as an unusual cause of restrictive motility disturbance. Surv Ophthalmol 1989;33:281– 284. 26. Doherty EJ, Macy ME, Wang SM, Dykeman CP, Melanson MT, Engle EC. CFEOM3: a new extraocular congenital ﬁbrosis syndrome that maps to 16q24.2–q24.3. Investig Ophthalmol Vis Sci 1999;40(8): 1687–1694. 27. Drummond GT, Keech RV. Absent and anomalous superior oblique and superior rectus muscles. Can J Ophthalmol 1989;24(6):275–279. 28. Effron L, Price RL, Berlin AJ. Congenital unilateral orbital ﬁbrosis with suspected prenatal orbital penetration. J Pediatr Ophthalmol Strabismus 1985;22(4):133–136. 29. Egbert J, May K, Kersten R, Kulwin D. Pediatric orbital ﬂoor fracture: direct extraocular muscle involvement. Ophthalmology 2000; 107:1875–1879. 30. Egbert JE, Anderson JH, Summers CG. Increased duration of low retinal slip velocities following retroequatorial placement of horizontal recti. J Pediatr Ophthalmol Strabismus 1995;32(6):359–363.

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31. Eitzen JP, Elsas FJ. Strabismus following endoscopic intranasal sinus surgery. J Pediatr Ophthalmol Strabismus 1991;28(3):168–170. 32. Engle EC, Goumnerov BC, McKeown CA, et al. Oculomotor nerve and muscle abnormalities in congenital ﬁbrosis of the extraocular muscles. Ann Neurol 1997;41(3):314–325. 33. Engle EC, Marondel I, Houtman WA, et al. Congenital ﬁbrosis of the extraocular muscles (autosomal dominant congenital external ophthalmoplegia): genetic homogeneity, linkage reﬁnement, and physical mapping on chromosome 12. Am J Hum Genet 1995;57(5): 1086–1094. 34. Engle EC, Kunkel LM, Specht LA, Beggs AH. Mapping a gene for congenital ﬁbrosis of the extraocular muscles to the centromeric region of chromosome 12. Nat Genet 1994;7(1):69–73. 35. Brodsky MC, Fray KJ. Surgical management of intermittent exotropia with high AC/A ratio. J Am Assoc Pediatr Ophthalmol Strabismus 1998;2:330–332. 36. Fioretto M, Burtolo C, Fava GP. New surgical method for nystagmus without null point. Ophthalmologica 1991;203(4):180–183. 37. Flaherty MP, Grattan-Smith P, Steinberg A, Jamieson R, Engle EC. Congenital ﬁbrosis of the extraocular muscles associated with cortical dysplasia and maldevelopment of the basal ganglia. Ophthalmology 2001;108(7):1313–1322. 38. Fujii GY, Kah-Guan AE, Pieramici DJ, et al. Macular translocation: unifying concepts, terminology, and classiﬁcation. Am J Ophthalmol 1992;114:72–80. 39. Gillies WE, Harris AJ, Brooks AM, Rivers MR, Wolfe RJ. Congenital ﬁbrosis of the vertically acting extraocular muscles. A new group of dominantly inherited ocular ﬁbrosis with radiologic ﬁndings. Ophthalmology 1995;102(4):607–612. 40. Grimmet MR, Lambert S. Superior rectus overcorrection after cataract extraction. Am J Ophthalmol 1992;114:72–80. 41. Goldberg AB, Greenberg MB, Darney PD. Misoprostol and pregnancy. N Engl J Med 2001;344(1):38–47. 42. Greenberg MF, Pollard ZF. Absence of multiple extraocular muscles in craniosynostosis. J Am Assoc Pediatr Ophthalmol Strabismus 1998;2(5):307–309. 43. Guemes A, Wright KW. Effect of graded anterior transposition of the inferior oblique muscle on versions and vertical deviation in primary position. J Am Assoc Pediatr Ophthalmol Strabismus 1998;2(4):201– 206. 44. Gusek-Schneider GC, Langenbucher A, Seitz B. Association of keratoconus and Möbius’ syndrome. J Pediatr Ophthalmol Strabismus 2001;38(1):47–48. 45. Guyton DL. Dissociated vertical deviation: etiology, mechanism, and associated phenomena. Costenbader lecture. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(3):131–144. 46. Hamed, Mancuso. Inferior rectus muscle contracture syndrome after retrobulbar anesthesia. Ophthalmology 1991;98:1506–1512.

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47. Hamlet YJ, Goldstein JH, Rosenbaum JD. Dehiscence of lateral rectus muscle following intrascleral buckling procedure. Ann Ophthalmol 1982;14:694–697. 48. Harley RD, Rodrigues MM, Crawford JS. Congenital ﬁbrosis of the extraocular muscles. J Pediatr Ophthalmol Strabismus 1978;15(6): 346–358. 49. Harley RD, Rodrigues MM, Crawford JS. Congenital ﬁbrosis of the extraocular muscles. Trans Am Ophthalmol Soc 1978;76:197–226. 50. Hayashi T, Iwashige H, Maruo T. Clinical features and surgery for acquired progressive esotropia associated with severe myopia. Acta Ophthalmol Scand 1999;77(1):66–71. 51. Hertel RW, Katowitz JA, Young PL, et al. Congenital unilateral ﬁbrosis, blepharoptosis, and enophthalmos syndrome. Ophthalmology 1992;99:347–355. 52. Holmes JM, Beck RW, Kip KE, Droste PJ, Leske DA. Predictors of nonrecovery in acute traumatic sixth nerve palsy and paresis. Ophthalmology 2001;108(8):1457–1460. 53. Holmes JM, Beck RW, Kip KE, Droste PJ, Leske DA. Botulinum toxin treatment versus conservative management in acute traumatic sixth nerve palsy or paresis. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(3):145–149. 54. Hotchkiss MG, Miller NR, Clark AW, et al. Bilateral Duane’s retraction syndrome: a clinical-pathologic case report. Arch Ophthalmol 1980;98:870–874. 55. Huber A. Electrophysiology of the retraction syndromes. Br J Ophthalmol 1974;58:293–300. 56. Hudson HL, Feldon SE. Late overcorrection of hypotropia in Grave’s ophthalmopathy. Ophthalmology 1992;99:356–360. 57. Hwang JM, Wright KW. Combined study on the causes of strabismus after retinal surgery. Korean J Ophthalmol 1994;8(2):83–91. 58. Ingham PN, McGovern ST, Crompton JL. Congenital absence of the inferior rectus muscle. Aust NZ J Ophthalmol 1986;14(4):355–358. 59. Jameson NA, Good WV, Hoyt CS. Fat adherence simulating inferior oblique palsy following blepharoplasty. Arch Ophthalmol 1992; 110(10):1369. 60. Kalpakian B, Bateman JB, Sparkes RS, Wood GK. Congenital ocular ﬁbrosis syndrome associated with the Prader–Willi syndrome. J Pediatr Ophthalmol Strabismus 1986;23(4):170–173. 61. Kanski JJ, Elkington AR, Davies MS. Diplopia after retinal detachment surgery. Am J Ophthalmol 1973;76:38–40. 62. Kodsi SR, Younge BR. Acquired oculomotor, trochlear, and abducent cranial nerve palsies in pediatric patients. Am J Ophthalmol 1992; 114(5):568–574. 63. Krzizok TH, Kaufmann H, Traupe H. New approach in strabismus surgery in high myopia. Br J Ophthalmol 1997;81:625–630. 64. Krzizok TH, Schroeder BU. Measurement of recti eye muscle paths by magnetic resonance imaging in highly myopic and normal subjects. Investig Ophthalmol Vis Sci 1999;40(11):2554–2560.

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65. Lee J, et al. Results of a prospective randomized trial of botulinum toxin therapy in acute unilateral sixth nerve palsy. J Pediatr Ophthalmol Strabismus 1994;31:283–286. 66. Lengyel D, Zaunbauer W, Keller E, Gottlob I. Mobius syndrome: MRI ﬁndings in three cases. J Pediatr Ophthalmol Strabismus 2000;37(5): 305–308. 67. Lin PY, Yen MY. Congenital absence of bilateral inferior rectus muscles: a case report. J Pediatr Ophthalmol Strabismus 1997;34(6): 382–384. 68. Lueder GT, Scott WE, Kutschke PJ, Keech RV. Long-term results of adjustable suture surgery for strabismus secondary to thyroid ophthalmopathy. Ophthalmology 1992;99(6):993–997. 69. Mark LE, Kennerdell JS. Medial rectus injury from intranasal surgery. Arch Ophthalmol 1979;97(3):459–461. 70. Mets MB, Parks MM, Freeley DA, Cornell FM. Congenital absence of inferior rectus muscle: report of three cases and their management. Binoc Vis 1987;2(2):77–86. 71. Mets MB, Wendell ME, Gieser RG. Ocular deviation after retinal detachment surgery. Am J Ophthalmol 1985;99:667–672. 72. Metz HS, Norris A. Cyclotorsional diplopia following retinal detachment surgery. J Pediatr Ophthalmol Strabismus 1987;24(6): 287–290. 73. Metz HS. Double elevator palsy. Arch Ophthalmol 1979;97:901– 909. 74. Metz HS, Dickey CF. Treatment of unilateral acute sixth nerve palsy with botulinum toxin. Am J Ophthalmol 1991;112:381–384. 75. Michel O, Oberlander N, Neugebauer P, Neugebauer A, Russmann W. Follow-up of transnasal orbital decompression in severe Graves’ ophthalmopathy. Ophthalmology 2001;108(2):400–404. 76. Miller NR, Kiel SM, Green WR, Clark AW. Unilateral Duane’s retraction syndrome. Arch Ophthalmol 1982;100:1468–1472. 77. Mitchell PR, Wheeler MB, Parks MM, Kestenbaum surgical procedure for torticollis secondary to congenital nystagmus. J Pediatr Ophthalmol Strabismus 1987;24(2):87–93. 78. Munoz M, Rosenbaum AL. Long-term strabismus complications following retinal detachment surgery. J Pediatr Ophthalmol Strabismus 1987;24(6):309–314. 79. Nakano M, Yamada K, Fain J, et al. Homozygous mutations in ARIX (PHOX2A) result in congenital ﬁbrosis of the extraocular muscles type 2. Nat Genet 2001. 80. Nardi M, Barca L. Hypercorrection of hypotropia in Graves’ ophthalmopathy. Ophthalmology 1993Jan;100(1):1–2. 81. Neely DE, Helveston EM, Thuente DD, Plager DA. Relationship of dissociated vertical deviation and the timing of initial surgery for congenital esotropia. Ophthalmology 2001;108(3):487–490. 82. Neugebauer A, Fricke J, Kirsch A, Russmann W. Modiﬁed transposition procedure of the vertical recti in sixth nerve palsy. Am J Ophthalmol 2001;131(3):359–363.

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83. Oh SY, Clark RA, Velez F, Demer JL. Magnetic resonance imaging demonstration of instability of rectus pulleys as cause of incomitant strabismus. Investig Ophthalmol Vis Sci 2001;167:42–44. 84. Parks MM. Causes of the adhesive syndrome In: Symposium on strabismus. Transaction of the New Orleans Academy of Ophthalmology. St Louis: Mosby, 1978:269–279. 85. Pearlman JT, Christensen RE. Motility problems following retinal detachment surgery. Am Orthopt J 1972;22:64–67. 86. Pedraza S, Gamez J, Rovira A, et al. MRI ﬁndings in Möbius syndrome: correlation with clinical features. Neurology 2000;55(7): 1058–1060. 87. Peleg D, Nelson GM, Williamson RA, Widness JA. Expanded Möbius syndrome. Pediatr Neurol 2001;24(4):306–309. 88. Pinchoff BS, Sandall G. Congenital absence of the superior oblique tendon in craniofacial dysostosis. Ophthalmic Surg 1985;16(6):375– 377. 89. Porter JD, Baker RS. Absence of oculomotor and trochlear motoneurons leads to altered extraocular muscle development in the Wnt-1 null mutant mouse. Dev Brain Res 1997;100(1):121– 126. 90. Prata JA, Minckler DS, Green RL. Pseudo-Brown’s syndrome as a complication of glaucoma drainage implant surgery. Ophthalmic Surg 1993;24:608–611. 91. Prendiville P, Chopra M, Gauderman WJ, Feldon SE. The role of restricted motility in determining outcomes for vertical strabismus surgery in Graves’ ophthalmology. Ophthalmology 2000;107(3):545– 549. 92. Price RL, Pederzolli A. Strabismus following retinal detachment surgery. Am Orthopt J 1982;32:9–17. 93. Quinn AG, Kraft SP, Day C, Taylor RS, Levin AV. A prospective evaluation of anterior transposition of the inferior oblique muscle, with and without resection, in the treatment of dissociated vertical deviation. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(6):348– 353. 94. Raab EL. Clinical features of Duane’s syndrome. J Pediatr Ophthalmol Strabismus 1986;23:64–68. 95. Raina J, Wright KW, Lin MM, McVey JH. Effectiveness of lateral rectus Y split surgery for correcting the upshoot and downshoot in Duane’s retraction syndrome, Type III. Binoc Vis Strabismus 1997; 12(4):233–238. 96. Reck AC, Manners R, Hatchwell E. Phenotypic heterogeneity may occur in congenital ﬁbrosis of the extraocular muscles. Br J Ophthalmol 1998;82(6):676–679. 97. Reinecke RD. Retroequatorial placement of horizontal recti. J Pediatr Ophthalmol Strabismus 1996;33(3):201–202. 98. Rene C, Rose GE, Lenthall R, Moseley I. Major orbital complications of endoscopic sinus surgery. Br J Ophthalmol 2001;85(5):598–603 (review).

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99. Roberts EL, Saunders RA, Wilson ME. Surgery for vertical head position in null point nystagmus. J Pediatr Ophthalmol Strabismus 1996;33(4):219–224. 100. Rogers GL, Bremer DL. Surgical treatment of the upshoot and downshoot in Duane’s retraction syndrome. Ophthalmology 1984;91(11): 1380–1383. 101. Romano PE. Absent or hypoplastic extraocular muscles? J Med Genet 1989;26(3):216. 102. Rosenbaum A, Kushner BJ, Kirschen D. Vertical rectus muscle transposition and botulinum toxin (oculinum) to medial rectus for abducens palsy. Arch Ophthalmol 1989;107:820. 103. Roth AM, Sypnicki BA. Motility dysfunction following surgery for retinal detachment. Am Orthopt J 1975;25:118–121. 104. Saunders RA, Rogers CT. Superior oblique transposition for third nerve palsy. Ophthalmology 1982;89:310. 105. Schumacher-Feero LA, Yoo KW, Solari FM, Biglan AW. Third cranial nerve palsy in children. Am J Ophthalmol 1999;128(2):216– 221. 106. Scott WE, Jackson OB. Double elevator palsy: the signiﬁcance of inferior rectus restriction. Ophthalmology 1977;27:5–10. 107. Scott AB, Wong GY. Duane’s syndrome: an electromyographic study. Arch Ophthalmol 1972;87:142–147. 108. Seiff SR, Good WV. Hypertropia and the posterior blowout fracture: mechanism and management. Ophthalmology 1996;103(1):152– 156. 109. Sener EC, Lee BA, Turgut B, Akarsu AN, Engle EC. A clinically variant ﬁbrosis syndrome in a Turkish family maps to the CFEOM1 locus on chromosome 12. Arch Ophthalmol 2000;118(8):1090–1097. 110. Sewell JJ, Knobloch WH, Eifrig DE. Extraocular muscle imbalance after surgical treatment for retinal detachment. Am J Ophthalmol 1974;78:321. 111. Smiddy WE, Loupe D, Michels RG, et al. Extraocular muscle imbalance after scleral buckling surgery. Ophthalmology 1989;96:1485– 1490. 112. Smith SL, Starita RJ, Fellman RL, Lynn JR. Early clinical experience with the Baerveldt 350-mm2 glaucoma implant and associated extraocular muscle imbalance. Ophthalmology 1993;100:914–918. 113. Snir M, Gilad E, Ben-Sira I. An unusual extraocular muscle anomaly in a patient with Crouzon’s disease. Br J Ophthalmol 1982;66(4):253– 257. 114. Stager DR, Weakley DR, Stager D. Anterior transposition of the inferior oblique: anatomic assessment of the neurovascular bundle. Arch Ophthalmol 1992;110:360–362. 115. Strachan IM, Brown BH. Electromyography of extraocular muscles in Duane’s syndrome. Br J Ophthalmol 1972;56:594–599. 116. Taylor R, Whale K, Raines M. The heavy eye phenomenon: orthoptic and ophthalmic characteristics. Ger J Ophthalmol 1995;4:252– 255.

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117. Theodossiadis G, Nikolakis S, Apostolopoulos M. Immediate postoperative muscular disturbance in retinal detachment surgery. Mod Probl Ophthalmol 1979;20:367–372. 118. Traboulsi EI, Lee BA, Mousawi A, Khamis AR, Engle EC. Evidence of genetic heterogeneity in autosomal recessive congenital ﬁbrosis of the extraocular muscles. Am J Ophthalmol 2000;129(5):658– 662. 119. Trotter WL, Kaw P, Meyer DR, Simon JW. Treatment of subtotal medial rectus myectomy complicating functional endoscopic sinus surgery. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(4):250– 253. 120. Vargas FR, Schuler-Faccini L, Brunoni D, et al. Prenatal exposure to misoprostol and vascular disruption defects: a case-control study. Am J Med Genet 2000;95(4):302–306. 121. Varn MM, Saunders RA, Wilson ME. Combined bilateral superior rectus muscle recession and inferior oblique muscle weakening for dissociated vertical deviation. J Am Assoc Pediatr Ophthalmol Strabismus 1997;1(3):134–137. 122. von Noorden GK, Jenkins RH, Rosenbaum AL. Horizontal transposition of the vertical rectus muscles for treatment of ocular torticollis. J Pediatr Ophthalmol Strabismus 1993;30(1):8–14. 123. Wang SM, Zwaan J, Mullaney PB, et al. Congenital ﬁbrosis of the extraocular muscles type 2, an inherited exotropic strabismus ﬁxus, maps to distal 11q13. Am J Hum Genet 1998;63(2):517–525. 124. Wilcox LM, Gittinger JW, Breinen GM. Congenital adduction palsy and synergistic divergence. Am J Ophthalmol 1981;91:1–7. 125. Wilder WM, Williams JP, Hupp SL. Computerized tomographic ﬁndings in two cases of congenital ﬁbrosis syndrome. Comput Med Imaging Graph 1991;15(5):361–363. 126. Wilson WB, Prochoda M. Radiotherapy for thyroid orbitopathy. Effects on extraocular muscle balance. Arch Ophthalmol 1995; 113(11):1420–1425. 127. Wilson ME, Parks MM. Primary inferior oblique overaction in congenital esotropia: accommodative esotropia and intermittent exotropia. Ophthalmology 1989;96:952–957. 128. Wilson ME, Saunders RA, Berland JE. Dissociated horizontal deviation and accommodative esotropia: treatment options when an esoand an exodeviation co-exist. J Pediatr Ophthalmol Strabismus 1995; 32(4):228–230. 129. Wilson ME, McClatchey SK. Dissociated horizontal deviation. J Pediatr Ophthalmol Strabismus 1991;28(2):90–95. 130. Wolff SM. Strabismus after retinal detachment surgery. Trans Am Ophthalmol Soc 1983;81:182–192. 131. Wolff JE, Koutsandreou AC. Analysis of psychomotor development of ten children with Möbius syndrome. Dev Med Child Neurol 2001; 43(1):71–72. 132. Wright KW. Late overcorrection after inferior rectus recession. Ophthalmology 1996;103(9):1503–1507.

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133. Wright KW, Liu GY, Murphree AL, et al. Double elevator palsy, ptosis and jaw-winking. Am Orthopt J 1989;39:143–150. 134. Wright KW. The fat adherence syndrome and strabismus after retina surgery. Ophthalmology 1986;93:411–415. 135. Wright KW. Color atlas of strabismus surgery: strategies and techniques. Torrance, CA: Wright, 2000. 136. Wright KW, Edelman PM, McVey JH, Terry A, Lin M. High-grade stereoacuity after early surgery for congenital esotropia. Arch Ophthalmol 1994;112:913–919. 137. Wright KW. Clinical optokinetic nystagmus asymmetry in treated esotropes. J Pediatr Ophthalmol Strabismus 1996;33(3):153–155. 138. Yamada M, Shinoda K, Hatakeyama A, Nishina S, Mashima Y. Fat adherence syndrome after retinal surgery treated with amniotic membrane transplantation. Am J Ophthalmol 2001;132(2):280–282.

11 Strabismus Surgery Kenneth W. Wright and Pauline Hong

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his chapter discusses various strabismus surgery procedures and how they work. When a muscle contracts, it produces a force that rotates the globe. The rotational force that moves an eye is directly proportional to the length of the moment arm (m) (Fig. 11-1A) and the force of the muscle contraction (F) (Fig. 11-1B). Rotational force m F where m moment arm and F muscle force. Strabismus surgery corrects ocular misalignment by at least four different mechanisms: slackening a muscle (i.e., recession), tightening a muscle (i.e., resection or plication), reducing the length of the moment arm (i.e., Faden), or changing the vector of the muscle force by moving the muscle’s insertion site (i.e., transposition).

MUSCLE RECESSION A muscle recession moves the muscle insertion closer to the muscle’s origin (Fig. 11-2), creating muscle slack. This muscle slack reduces muscle strength per Starling’s length–tension curve but does not signiﬁcantly change the moment arm when the eye is in primary position (Fig. 11-3). The arc of contact of the rectus muscles wrapping around the globe to insert anterior to the equator of the eye allows for large recessions of the rectus muscles without signiﬁcantly changing the moment arm. Figure 11-3 shows a 7.0-mm recession of the medial and lateral rectus muscles. Note there is no change in the moment arm with these large recessions. Thus, the effect of a recession on eye position is determined by the amount of muscle slack created.1a The 388

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FIGURE 11-1A,B. (A) Diagram of the horizontal rectus muscles shows the relationship of the moment arm (m) to the muscle axis and center of rotation. The moment arm intersects the center of rotation and is perpendicular to the muscle axis. The longer the moment arm, the greater the rotational force. (B) Starling’s length–tension curve. The relationship of a muscle’s force is proportional to the tension on the muscle. More tension on a muscle increases muscle force and slackening a muscle reduces its force. Note that the relationship is exponential, not linear: toward the end of the curve, a small amount of slackening produces a disproportionately large amount of muscle weakening.

A B C FIGURE 11-2A–C. Drawing of rectus muscle recession (shaded muscle). The effect of the recession is greatest when the eye rotates toward the recessed muscle. (A) The eye rotates toward the recessed muscle, causing the recessed muscle to tighten, therefore reducing muscle slack. (B) A rectus muscle resection resulting in muscle slack. (C) The eye rotates toward the recessed muscle, and the muscle and the muscle slack increase.

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5.5

7.0 m

MR

FIGURE 11-3. Medial rectus muscle recession. Diagram shows normal insertion at 5.5 mm posterior to the limbus and a 7.0-mm medial rectus recession. In primary position, the moment arm (m) has not changed, so the effect of the recession is to create muscle slack rather than to change the moment arm.

amount of muscle slack is most accurately determined by measuring the recession from the muscle insertion.8 Note the exponential character of the length–tension curve, as there is a precipitous loss of muscle force at the end of the curve when muscle slack is increased (see Fig. 11-1B); this is why even small, inadvertent inaccuracies of large recessions (6– 7 mm) can cause dramatic changes in muscle force and result in an unfavorable outcome. Technical mistakes, such as allowing central muscle sag and not properly securing the muscle, can lead to large overcorrections. For example, each 0.5 mm of bilateral medial rectus recessions up to a recession of 5.5 mm

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will correct approximately 5 prism diopters (PD) of esotropia. However, for recessions greater than 5.5 mm, each additional 0.5 mm of recession results in 10 prism diopters of correction (see chart on inside cover). Thus, an overrecession of only 1.0 mm on a planned 6.0-mm bilateral medial rectus recession would result in a 20-prism diopter overcorrection. Figure 11-4 shows the proper rectus muscle recession, with the muscle well secured and no central muscle sag. The best way to prevent central muscle sag is to broadly splay the new insertion so it is approximately the same width as the original insertion. A rectus muscle recession has its greatest effect in the ﬁeld of action of the muscle. Figure 11-2 shows that muscle slack increases when the eye rotates toward the recessed muscle, thus reducing the rotational force on gaze toward the recessed muscle. In contrast, eye rotation away from the recessed muscle causes muscle slack to be reduced. In addition, on rotation away from the recessed muscle, the recessed muscle is inhibited (Sherrington’s law), minimizing the effect of the recession in this gaze. For example, a right medial rectus recession will produce an incomitant strabismus, with an exodeviation in primary position and a larger exodeviation in leftgaze with very little exodeviation in rightgaze. Induced incomitance can correct incomitant strabismus. If a patient has a small esotropia in primary position and a large esotropia in leftgaze, a right medial rectus recession would reduce the incomitance. Comitant strabismus, on the other hand, is best treated with bilateral symmetrical surgery. Recessions are routinely performed on rectus muscles but can also be performed on oblique muscles. Inferior oblique muscle recession is a popular procedure for weakening the inferior oblique muscle. Recession of the superior oblique tendon has also been described. It not only slackens the superior oblique tendon but also changes the function of the muscle. A recession of the superior oblique tendon collapses the normally broad insertion and moves the new insertion nasal and anterior to the globe’s equator. This alteration changes the function of the superior oblique muscle and can result in unpredictable outcomes, including postoperative limitation of depression. A more controlled way of slackening the superior oblique tendon without changing the functional mechanics of the tendon insertion is a tendon-lengthening procedure, such as the Wright silicone tendon expander.

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FIGURE 11-4A,B. (A) Drawing of rectus muscle recession with the muscle secured to sclera at the recession point posterior to the original insertion. Note that the new insertion is almost as wide as the original scleral insertion, and the new insertion is parallel to the original insertion. There is no central muscle sag. (B) Companion photograph shows a rectus muscle recession with no central sag because the new insertion is splayed as wide as the original insertion.

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Hang-Back Technique A hang-back recession suspends the muscle back, posterior to the scleral insertion, with a suture (Fig. 11-5). This technique has the advantage of excellent exposure and relatively easy needle passes through the thick anterior sclera. On the other hand, hang-back recessions are potentially less accurate than a ﬁxed recession. Small to medium-sized hang-back recessions of 3 to 6 mm tend to result in overcorrections because they have inherent central muscle sag (Fig. 11.5). On the other hand, large hang-back recessions, over 6 mm, tend to produce undercorrections because an otherwise normal muscle will not consistently retract more than 6 to 7 mm posterior to the insertion. The surgeon experienced with adjustable suture surgery knows it is difﬁcult to recess a rectus muscle more than 6 mm using an adjustable hang-back suture. Large hang-back recessions are

FIGURE 11-5. Hang-back recession. The suture is passed through sclera at the original insertion and the muscle is suspended posteriorly to achieve the recession. Inset: Note the caliper is measuring the planned recession; however, the muscle is overrecessed because of central sag. Central sag occurs because the new insertion is lax and not splayed as widely as the original insertion.

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possible if the muscle is tight and contracted, as in the case of thyroid-associated strabismus, congenital ﬁbrosis syndrome, or a slipped muscle. Indications for hang-back recessions include a recession over a retinal buckle, recession over an area of scleral ectasia, or large recessions, of a tight contracted muscle, if posterior exposure is difﬁcult. However, for routine strabismus surgery, the author (K.W.W.) prefers the ﬁxed recession so the muscle is secured at the desired recession point.

Adjustable Suture Technique Adjustable suture techniques allow movement of the muscle position after surgery when the patient is fully awake and the anesthesia has dissipated (Fig. 11-6). Unlike ﬁxed sutures, the adjustable suture technique allows for ﬁne-tuning of ocular alignment in the immediate postoperative period. The adjustable suture procedure is usually performed on recessions in two stages: in the ﬁrst stage, surgery is performed under either local or general anesthesia, and the muscle is placed on a suture in such a way that the muscle position can be adjusted later. The second stage, or adjustment phase, is performed when the patient is fully awake or after the local anesthetic has worn off (5 h for lidocaine) and the muscle function has returned to normal. In this phase, the muscle is adjusted to properly align the eyes and then permanently tied in place. The adjustment procedure must be performed within 24 to 48 h after the initial surgery while the muscle is still freely mobile. Later adjustments have not been recommended because the muscle rapidly adheres to the globe. However, successful in-ofﬁce reoperation within the ﬁrst week of surgery has been described.5 The muscle is sutured like a hang-back recession, but the suture is tied in a bowknot or secured by a sliding noose so the position of the

FIGURE 11-6A–C. (A) Bow tie adjustable suture technique. After the sutures have been passed through the scleral insertion, they are tied together in a single-loop bow tie. This bow tie can be untied postoperatively to adjust the muscle. (B) Noose adjustable suture. Sutures suspend the muscle posteriorly, and a noose around the sutures slides up and down to secure the muscle at the desired position. The ocular alignment is ﬁnetuned with the patient awake. The muscle placement is ﬁnalized by tying off the pole sutures, then trimming all loose sutures. (C) Companion photograph of (B) shows adjustable suture through fornix, with scleral traction suture holding the conjunctiva superiorly and exposing the adjustable suture.

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muscle can be easily changed (Fig. 11-6A–C). Adjustable sutures have limitations similar to hang-back recessions, with the maximum recession approximately 6 to 7 mm. Central sag occurs but, because the muscle position can be changed after surgery, this is usually not an issue. Plan on a slight overcorrection, as advancing an over-recessed muscle is easier than trying to increase the recession, especially if the recession is greater than 6 to 7 mm. The most important indication for an adjustable suture is complicated strabismus, including paralytic strabismus, largeangle strabismus, reoperations, and thyroid myopathy. In these situations, the standard tables for surgical measurements do not apply, and results with the ﬁxed-suture technique are unpredictable. In addition to the more complicated strabismus cases, many surgeons routinely use adjustable sutures on most cooperative adult patients, even those undergoing uncomplicated, horizontal surgery. Adjustable sutures are usually used with recession procedures, as adjustable tightening procedures are difﬁcult to perform. Patient selection is crucial for successful implementation of the adjustable suture technique. The adjustment procedure is somewhat uncomfortable and can evoke substantial anxiety. There is no speciﬁc age limitation for the use of adjustable sutures, but patients younger than 15 years of age are often too anxious about medical procedures. Unless a child is exceptionally calm and cooperative, adjustable sutures should be limited to cooperative adult patients. Strong sedatives before adjustment should be avoided because sedation inﬂuences eye position. The patient should wear full optical correction when ocular alignment is being assessed during the adjustment procedure to ensure proper image clarity and control of accommodation.

MUSCLE SHORTENING PROCEDURES Muscle shortening procedures include muscle resections, tucks, and plications. These procedures tighten the muscle, but they do not actually strengthen the muscle. For the most part, they correct strabismus by creating a tight muscle that acts like a leash or tether. These procedures produce incomitance, as the tightened muscle restricts rotation away from the shortened muscle (Fig. 11-7). For example, a right medial rectus shortening procedure limits abduction of the right eye and creates an

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A B C FIGURE 11-7A–C. Effect of a rectus muscle resection (shaded muscle). The resection has its greatest effect on gaze away from the resection. (A) The muscle tightens on gaze away from the resected muscle. (B) A resected rectus muscle. (C) The muscle slackens on gaze to the resected muscle.

esodeviation shift that increases in rightgaze. Right medial rectus tightening would be indicated to correct an incomitant exotropia that is greater in rightgaze. Note that tightening the medial rectus muscle does not strengthen adduction but instead limits abduction. Bilateral medial rectus resections limit divergence and induce an esodeviation greater for distance ﬁxation; therefore, it is not the answer for convergence insufﬁciency.

Resection A muscle resection consists of tightening a muscle by removing the anterior part of the muscle and reattaching the shortened muscle to the original insertion site. The muscle resection is the most popular tightening procedure and is performed on rectus muscles.

Tuck A muscle tuck shortens the muscle by folding the muscle and suturing the folded muscle to muscle. The muscle tuck has, for the most part, fallen out of favor partially because the muscleto-muscle suturing does not hold well and tends to become cheese-wire loose over time. A superior oblique tendon tuck or plication, however, is used for some cases of superior oblique

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palsy, either as a full-tendon plication or plication of the anterior tendon ﬁbers (i.e., Harada–Ito procedure).

Wright Plication The author (K.W.W.) developed a rectus muscle plication procedure that tightens the muscle by folding the muscle and suturing it to sclera (Fig. 11-8).14,18 With the plication, the muscle is sutured to the scleral insertion, in contrast to a tuck, where muscle is sutured to muscle. The muscle–scleral attachment of

A

B FIGURE 11-8A,B. Wright rectus muscle plication. (A) The muscle is secured with the suture placed posterior to the insertion at the desired plication point (usually 6 mm or less). Once the posterior muscle is secured, the suture ends are passed through the scleral insertion. The drawing shows the suture secured to the posterior muscle and the doublearmed needles being passed at the scleral insertion. (B) The plication is completed with the posterior muscle advanced to the insertion. There is a small roll of redundant tendon that will ﬂatten and disappear 3 to 4 weeks after surgery.

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the plication is more secure than the muscle-to-muscle union of a tuck. The plication can be used in place of a standard resection. Because there is a fold of tendon associated with the plication, a small lump is present immediately after surgery but disappears within 3 to 4 weeks. Important advantages of the plication procedure over resection include reversibility. A plication can be removed by simply cutting and removing the suture within 2 days of the surgery, before the muscle heals to sclera. Another advantage is safety against a lost muscle. Because the muscle is not disinserted, there is little risk of a lost muscle. The plication procedure also preserves the anterior ciliary vessels and reduces the risk of anterior segment ischemia. These advantages have made the Wright plication popular for small or mediumsized rectus muscle tightening surgeries.

RECESSION AND RESECTION Resections (or plications) of rectus muscles can be teamed with a recession of the antagonist muscle same eye to correct strabismus. This monocular surgery is called a recession–resection, or “R & R,” procedure. The effect of the recession–resection of agonist and antagonist induces incomitance and limits ocular rotation in one direction. For example, a right lateral rectus muscle recession reduces ocular rotation to the right, and a resection of the right medial rectus muscle also restricts rotation to the right. Limited rotations after an R & R procedure may improve over several months to years, but some residual incomitance often persists. Because the R & R procedure induces incomitance, it can be used to treat incomitant strabismus. It is also useful in treating sensory strabismus, allowing monocular surgery to be performed only on the amblyopic eye and sparing surgery to the good eye.

FADEN The Faden procedure is performed by suturing the rectus muscle to sclera, 12 to 14 mm posterior to the rectus muscle insertion. This technique pins the rectus muscle to the sclera so, when the eye rotates toward the fadened muscle, the arc of contact cannot unravel. As a result, the moment arm shortens, thus reducing

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the rotational force. The Faden, however, does not signiﬁcantly change the moment arm when the eye is in primary position, and it has no effect when the eye is turned away from the muscle with the Faden (Fig. 11-9). Thus, a Faden reduces ocular rotational force when the eye rotates toward the fadened muscle and is used to correct incomitant strabismus. The weakening effect of the Faden operation by itself is relatively small, so the fadened muscle is usually also recessed as part of the Faden procedure. The Faden operation works best on the medial rectus muscle because the medial rectus muscle has the shortest arc of contact (approximately 6 mm), and a 12- to 14-mm Faden signiﬁcantly changes its arc of contact. Alternately, a Faden of the lateral rectus muscle has little effect because the arc of contact is 10 mm, and pinning the muscle at 12 mm does not signiﬁcantly change this naturally long arc of contact. For the most part, the Faden operation is indicated to correct incomitant esotropia by enhancing the effect of a medial rectus recession, such as in the case of sixth nerve paresis or high AC/A esotropia. The following case is an example where a

A FIGURE 11-9A. Faden of rectus muscle. (A) In primary position, the Faden does not signiﬁcantly change the moment arm (m).

FIGURE 11-9B–C. (B) Ocular rotation toward the Faden results in shortening of the moment arm (m) as the muscle is pinned to sclera. (C) On rotation away from the Faden, the moment arm (m) is normal and the faden has no signiﬁcant effect. Thus, the Faden weakens the muscle on rotation toward the fadened muscle.

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Faden and recession of the right medial rectus muscle is indicated. One may rightfully argue, however, that a large (5-mm) right medial rectus muscle recession would also work without the difﬁculty of performing the Faden. As you will see, there is often more than one way to approach a strabismus. Rightgaze Orthotropia

Primary position

Leftgaze

E4

ET 10

ET, esotropia. Surgery: recess the right medial rectus muscle 3 mm with a Faden.

Sixth Nerve Paresis An example where the Faden may be effective is a partial sixth nerve paresis and good lateral rectus function. The standard surgery has historically been a recession of the medial rectus muscle and resection of the lateral rectus muscle of the paretic eye, which helps correct the esodeviation in primary position but does not address the large esotropia that occurs with gaze to the side of the paretic lateral rectus muscle. Incomitance can be improved with a recession and a Faden operation of the contralateral medial rectus muscle. A Faden to the contralateral medial rectus muscle helps correct the esotropia that increases in the side of the paretic lateral rectus muscle by decreasing the rotational force of the yoke medial rectus, thus matching the paretic lateral rectus muscle. Matching yoke muscles only works if there is good lateral rectus function with no more than 1 limitation of abduction.

High AC/A Ratio Esotropia Theoretically, the Faden operation reduces convergence at near, thus lowering the AC/A ratio. Experience with this procedure indicates that most patients still require a bifocal add to obtain fusion at near. Augmented bilateral medial rectus recessions probably work just as well.7 The use of a Faden operation with a medial rectus recession in high AC/A ratio esotropia patients remains controversial.

MUSCLE TRANSPOSITION PROCEDURES Transposition surgery is based on changing the location of the muscle insertion so the muscle pulls the eye in a different direction (i.e., changes the vector of force). Transposition surgeries

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can be used to treat A- and V-patterns, small vertical tropias, rectus muscle paresis, and torsion.

Horizontal Muscle Transposition for Aand V-Patterns See Chapter 9: A- and V-Patterns and Oblique Dysfunction.

Transposition for Small Vertical Deviations Transposition surgery can correct small vertical deviations by vertically offsetting the horizontal rectus muscles. A patient with an esotropia and a small right hypertropia, for example, can be corrected by a recession–resection procedure of the right eye with inferior infraplacement of the horizontal rectus muscles. By transposing the horizontal rectus muscles inferiorly, they act to pull the eye down, thus correcting the hypertropia. Each horizontal muscle is recessed or resected as speciﬁed by the magnitude of the horizontal deviation. There is approximately 1 prism diopter of improvement in the vertical deviation per 1 mm of displacement; this is true when two muscles in the same eye are transposed in the same direction. Vertical muscle displacements as large as 6 to 7 mm may be readily performed with this technique. It is most useful when the surgeon is performing monocular recession–resection surgery in which both muscles are moved in the same direction (Fig. 11-10). This surgery, however, is not effective if restriction is present (e.g., thyroid orbitopathy).

FIGURE 11-10. Full-tendon-width inferior transposition of both horizontal rectus muscles. The muscle on the left has been resected and infraplaced; the muscle on the right has been recessed and infraplaced. This technique would be used with a recession/resection procedure to correct a hypertropia and horizontal strabismus.

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Transposition Procedures for Rectus Muscle Palsy Three transposition procedures used to correct severe rectus muscle palsies are described here: Knapp, Jensen, and Hummelsheim. In a right lateral rectus palsy, there is limited abduction and a large esotropia that increases in rightgaze. If there is less than 50% lateral rectus function, the treatment should be a lateral transposition of all or part of the superior and inferior rectus muscles. Because the vertical muscles do not contract on attempted abduction, the amount of abduction would relate to the elasticity or tonic contraction of the transposed muscles, rather than the active contraction of the transposed muscles.

KNAPP PROCEDURE A full-tendon transfer, or Knapp procedure, was originally described for the management of double elevator palsy. This procedure, however, can also be used for a sixth nerve palsy. The key for successful surgery is symmetrical transposition to avoid induced vertical or horizontal deviations. A large posterior dissection to free the muscle of the intermuscular septum and check ligaments is necessary to mobilize the muscle for the tendon transfer (Fig. 11-11).

JENSEN PROCEDURE The Jensen procedure is a split-tendon transfer with the adjacent muscle tied together but not disinserted (Fig. 11-12). This procedure has the advantage of leaving the anterior ciliary arteries intact, diminishing the risk of anterior segment ischemia. Even with the Jensen procedure, however, some vascular compromise occurs, and anterior segment ischemia has been associated with this procedure.

HUMMELSHEIM PROCEDURE The Hummelsheim procedure is a split-tendon transposition technique designed to preserve anterior ciliary artery perfusion. Half of each of the two rectus muscles adjacent to the weak muscle is mobilized. The halves are then transposed and inserted at the insertion of the weak or lost muscle (Fig. 11-13). In contrast to the Jensen procedure, the Hummelsheim procedure can be used for a lost muscle, as it does not require the

FIGURE 11-11. Knapp procedure. The medial rectus (MR) and lateral rectus (LR) muscles are transposed superiorly to the insertion of the superior rectus (SR) muscle.

FIGURE 11-12. Jensen procedure. Nonabsorbable sutures tie muscle halves from adjacent muscles. The ﬁnal result shows the tendon unions of superior rectus to lateral rectus and inferior rectus to lateral rectus muscles. The posterior location of the union is important, and sutures should be at least 12 mm posterior to the insertions. Anterior union sutures will reduce the effect of the transposition.

FIGURE 11-13. Hummelsheim procedure. Half of each of the superior and inferior rectus muscles is transposed to the lateral rectus insertion. Note that the transposed muscle halves touch the lateral rectus insertion, and the muscles are sutured together 3 mm posterior to the insertion (Foster modiﬁcation).

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presence of the weak muscle. The Hummelsheim procedure is the author’s procedure of choice for a muscle palsy.

MODIFICATION

OF THE

HUMMELSHEIM

Two modiﬁcations of the Hummelsheim procedure, which increase the effect of the transposition, are described here. Augmented Hummelsheim Brooks of Augusta, Georgia, has augmented the Hummelsheim by resecting 4 to 6 mm of the transposed rectus muscle halves. Resecting some of the transposed muscle halves tighten the transposition, increasing the leash effect. Muscle Union Modiﬁcation (Foster modiﬁcation) Increased effect of the Hummelsheim has been suggested if the transposed muscle is sutured to the paretic muscle. The transposed and paretic muscles are sutured together and then to sclera, 4 mm posterior the insertion.

Complications of Transposition Surgery Transposition procedures for rectus muscle palsies can induce unwanted deviations if there is asymmetrical muscle placement. In split-tendon procedures, it is important to split and transpose the muscle equally to prevent inadvertent deviations. Anterior segment ischemia is always an important consideration. Split-tendon procedures such as the Jensen and Hummelsheim lessen the risks, but even these procedures have been associated with anterior segment ischemia. The best strategy is to preserve as many anterior ciliary arteries as possible. A limbal conjunctival incision disrupts local vessels and may increase the risk of anterior segment ischemia, suggesting that a fornix incision may be preferable.

Rectus Muscle Transposition for Torsion Torsional strabismus can be improved by moving vertical rectus muscles nasally or temporally. Nasal placement of the superior rectus causes extorsion (corrects intorsion) whereas temporal placement causes intorsion (corrects extorsion). The opposite is true for the inferior rectus muscle, with nasal transposition induces intorsion (corrects extorsion) and temporal transposition induces extorsion (corrects intorsion). Transposition of a

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tendon width (approximately 7 mm) will induce about 4° to 5° of torsion. Most of the torsional effect is seen in the ﬁeld of action of the transposed muscle. If the superior rectus muscle is nasally transposed 7 mm and the inferior rectus muscle temporally transposed 7 mm, a total of 8° to 10° of extorsion would be induced, thus correcting 8° to 10° of intorsion. Horizontal rectus muscle transposition will also produce some torsional changes, but less than vertical rectus muscle transpositions. Supraplacement of the medial rectus muscle induces intorsion; infraplacement induces extorsion. The opposite is true for the lateral rectus muscle. It is unusual for a vertical transposition of a horizontal muscle to induce signiﬁcant torsion. Most cases of torsional strabismus are caused by oblique dysfunction and are best treated with oblique muscle surgery to correct the torsion. For example, extorsion associated with bilateral superior oblique paresis is usually best handled with a bilateral Harada–Ito procedure, not a rectus muscle transposition.

INFERIOR OBLIQUE MUSCLE WEAKENING PROCEDURES Surgical management of inferior oblique muscle overaction is based on weakening or changing the function of the inferior oblique muscle. Techniques include myectomy, recession, and anterior transposition. Inferior oblique myotomy is not effective because the cut ends of the muscle inevitably reunite or scar to sclera; this causes residual inferior oblique overaction and an unacceptably high reoperation rate. Myectomy weakens the inferior oblique, as removing a portion of muscle reduces the chance of local reattachment. A very large myectomy with surgical transection of the neurovascular bundle virtually eliminates inferior oblique overaction and is termed inferior oblique extirpation–denervation. Extirpation–denervation may be indicated for severe residual inferior oblique overaction after previous inferior oblique surgery. An inferior oblique recession places the insertion closer to the origin and induces muscle slack, thus reducing muscle tension (Fig. 11-14). Apt1 and Elliot4 were the ﬁrst to describe the inferior oblique anterior transposition. It is similar to a recession, but the inferior oblique muscle insertion is moved anterior to its origin, thus changing the function of the inferior oblique muscle from an elevator to more of a depressor

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FIGURE 11-14. Inferior oblique recession. The muscle is reattached along the path of the inferior oblique, but closer to its origin, thus slackening the muscle.

(Fig. 11-15). The more anterior the placement of the inferior oblique muscle insertion, the more the muscle becomes a depressor. This procedure has been shown to be very effective for treating both primary inferior oblique overaction and inferior oblique overaction secondary to superior oblique palsy.6 One possible complication of the anteriorization procedure is postoperative limited elevation. Limited elevation usually occurs from three possible mechanisms: (1) the new insertion is too anterior (i.e., anterior to the inferior rectus insertion); (2) resection of too much muscle (3 mm) at the time of securing

FIGURE 11-15. Inferior oblique anterior transposition. The diagram shows placement of the inferior oblique (IO) muscle in relationship to the inferior rectus (IR) insertion. The inferior oblique muscle is placed 1 mm posterior to the inferior rectus insertion. Note that the posterior inferior oblique muscle ﬁbers are placed posterior to the anterior ﬁbers and parallel to the inferior rectus muscle (no J-deformity).

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and disinserting the inferior oblique muscle; and (3) anterior placement of the posterior ﬁbers of the inferior oblique muscle. Stager described this last mechanism as a common cause for limited elevation after the anterior transposition procedure. The posterior ﬁbers of the inferior oblique muscle are important, as the neurovascular bundle of the muscle inserts into these muscle ﬁbers. Because the neurovascular bundle is inelastic, large anteriorizations of the posterior muscle ﬁbers will create a J-deformity of the muscle, with the neurovascular bundle tethering the inferior oblique muscle and limiting elevation of the eye (Fig. 11-16).12a To prevent postoperative limitation of elevation, the author (K.W.W.) recommends:

FIGURE 11-16. Full anteriorization of the inferior oblique muscle including the posterior ﬁbers with J-deformity. Anteriorization of the posterior ﬁbers creates the J-deformity, as the neuroﬁbrovascular bundle tethers the posterior muscle ﬁbers; this can limit elevation of the eye. Because of this complication, the author (K.W.W.) does not perform the “J” deformity anteriorization, except if performed bilaterally for severe dissociated vertical deviation (DVD) and inferior oblique overaction.

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1. Keep the new insertion at or behind the inferior rectus insertion. 2. Secure the muscle close to its insertion to avoid resecting too much muscle (this would shorten the muscle). 3. Avoid the “J” deformity by keeping the posterior muscle ﬁbers posterior to the anterior muscle ﬁbers and posterior to the inferior rectus muscle insertion by at least 3 mm.8,14 The full anteriorization with a “J” deformity has been used for the treatment of bilateral dissociated vertical deviation (DVD) with inferior oblique overaction. If performed, the full anteriorization with “J” deformity should be performed bilaterally to avoid asymmetrical elevation of the eyes.

Graded Recession–Anteriorization The author (K.W.W.) has reported on a graded recession– anteriorization approach for the management of inferior oblique overaction.8,14 This procedure tailors the amount of anteriorization according to the amount of inferior oblique overaction. The basis of the graded anteriorization procedure is that the more anterior the inferior oblique insertion, the greater the weakening affect. Table 11-1 lists the inferior oblique placement for a speciﬁc amount of inferior oblique overaction and represents only a guideline for the management of inferior oblique overaction. The ﬁnal surgical decision must be based on a combination of factors, including the amount of V-pattern and the presence of a vertical deviation in primary position. Asymmetrical graded anteriorization is indicated if a hypertropia is present in primary position; otherwise, consider symmetrical surgery. More anteriorization of the inferior oblique should be done on the side of the hyperdeviation. A full anteriorization (without J-deformity) on the side of the hypertropia and 4 mm anteriorization on the opposite side will correct approximately 6 prism diopters (PD) of hypertropia. In the case of a unilateral

TABLE 11-1. Graded Recession–Anteriorization of Inferior Oblique Muscle. Overaction

Inferior oblique placement

1 2 3 4

4 mm posterior and 2 mm lateral to inferior rectus (IR) insertion 3 mm posterior to IR insertion 1–2 mm posterior to IR insertion At the IR insertion

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inferior oblique overaction (e.g., associated with congenital superior oblique paresis), a unilateral anteriorization of 1 mm will correct approximately 8 to 12 PD of hypertropia.

COMPLICATIONS Limited elevation after inferior oblique anteriorization has been discussed previously, but another problem of inferior oblique surgery is persistence or recurrence of the overaction. A common cause of residual overaction is incomplete isolation of the inferior oblique muscle, leaving posterior ﬁbers intact. It is important to explore posteriorly along the globe for bridging muscle ﬁbers that would indicate missed inferior oblique ﬁbers. Weakening procedures of the inferior oblique muscle for primary overaction only rarely produce a postoperative torsional diplopia. Even so, an adult patient may complain of a transient excyclodiplopia after weakening of the inferior oblique muscle. An important anatomic consideration is the proximity of the inferior oblique muscle insertion to the macula. A misadventure with a stray needle in this area can cause the loss of central vision. Another consideration is the course of the inferior temporal vortex vein, which lies underneath the inferior oblique and can be inadvertently traumatized during surgery. The proximity of extraconal fat to the inferior oblique muscle is also an important concern, and fat adherence syndrome should be kept in mind; this may occur when the inferior oblique muscle is approached blindly and posterior Tenon’s capsule is violated. Other possible complications of inferior oblique surgery include orbital hemorrhage, pupillary dilation, endophthalmitis, and inadvertent surgery or damage to the lateral rectus muscle.11 Paramount in avoiding these complications is the clear and direct visualization of the inferior oblique muscle during its isolation. Blind hooking procedures must be avoided. Meticulous surgical dissection and hemostasis are the key to proper exposure and visualization of the anatomy.

SUPERIOR OBLIQUE MUSCLE TIGHTENING PROCEDURES The superior oblique tendon can be functionally divided into the anterior third, responsible for intorsion, and posterior twothirds, responsible for depression and abduction (Fig. 11-17).

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FIGURE 11-17. Diagram of superior oblique tendon insertion. The anterior ﬁbers are responsible for intorsion and the posterior ﬁbers for abduction and depression.

Tightening the anterior ﬁbers will induce intorsion without too much change in the depression and abduction functions of the superior oblique muscle; this is the basis of the Harada–Ito procedure, which is used for correcting extorsion. Tightening the full tendon is termed a superior oblique tuck or plication.

Harada–Ito Procedure The Harada–Ito procedure is commonly used to treat extorsion associated with a partially recovered acquired superior oblique palsy, where the residual strabismus is only extorsion. Tightening the entire tendon will result in depression and abduction and often produces an iatrogenic Brown’s syndrome. Therefore, the Harada–Ito has the advantage of correcting extorsion without causing a signiﬁcant Brown’s syndrome. Figure 11-18 shows two techniques for tightening the anterior ﬁbers: Figure 11-18A

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shows the disinsertion technique and Figure 11-18B shows a classic Harada–Ito procedure. The author prefers the classic Harada–Ito procedure because it is reversible by simply cutting the pullover suture.

Full-Tendon Tuck or Plication The superior oblique tuck or plication is reserved for severe bilateral superior oblique underaction where the tendon is lax, usually associated with either a congenital or trauma-induced palsy. A full-tendon tuck or plication tightens both anterior and posterior ﬁbers and enhances all three functions of the superior oblique muscle (Fig. 11-19). Tightening of the entire superior oblique tendon may improve its function slightly, but this will consistently cause an iatrogenic Brown’s syndrome or limited elevation in adduction. Care must be taken to balance the superior oblique tightening against the induced Brown’s syndrome by performing intraoperative forced ductions of the superior oblique after tucking or plicating. The amount of tuck or plication should be readjusted appropriately. This author (K.W.W.)

A B FIGURE 11-18A,B. Harada–Ito procedure: (A) With the disinsertion technique, the anterior ﬁbers of the superior oblique tendon are sutured, then disinserted, and moved anteriorly and laterally to be secured to sclera at a point 8 mm posterior to the superior border of the lateral rectus insertion. Lateralizing the anterior ﬁbers intorts the eye, thus correcting extorsion. (B) In the classic Harada–Ito procedure, the anterior superior oblique tendon ﬁbers are looped with a suture and displaced laterally without disinsertion. The anterior superior oblique tendon ﬁbers are sutured to sclera 8 mm posterior to the superior border of the lateral rectus muscle.

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FIGURE 11-19. Superior rectus tuck or plication. Inset—Sutures are placed in the nasal tendon, then passed through sclera at the insertion. The tendon is pulled to plicate the tendon.

reserves the superior oblique plication for those rare cases of congenital superior palsy caused by a lax superior oblique tendon, or severe bilateral traumatic superior oblique palsy with severe extorsion and esotropia in downgaze. Bilateral medial rectus recessions with infraplacement usually accompany the plications.

SUPERIOR OBLIQUE MUSCLE WEAKENING PROCEDURES Superior oblique weakening procedures are used in the management of superior oblique overaction and Brown’s syndrome.19 Various weakening procedures have been described including tenotomy, tenectomy, recession, split-tendon lengthening, and Z-lengthening of the superior oblique tendon. The split-tendon lengthening procedure works well but is difﬁcult to perform and has the disadvantage of causing tendon scarring. The superior

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oblique recession also creates a new insertion site nasal to the superior rectus muscle, changing the superior oblique muscle function from a depressor to an elevator. Limited depression has been described as a complication of the recession procedure. The superior oblique tenotomy has been popular, but it is an uncontrolled procedure and the tendon ends can separate, resulting in palsy, or grow back together, causing an undercorrection. A suture bridge has been used to prevent separation of the tendon ends, but the suture can act as scaffolding, allowing the tendon to grow back together. The author (K.W.W.) has developed a procedure to lengthen the superior oblique tendon, the Wright superior oblique tendon expander. This procedure has been very effective in treating superior oblique overaction and especially treating Brown’s syndrome.17

Superior Oblique Tenotomy Superior oblique tenotomy should be performed nasal to the superior rectus muscle (Fig. 11-20). Guyton’s exaggerated forced ductions should be performed after tenotomy to verify that the full tendon was found and tenotomized. Temporal tenotomies usually have minimal effect, as the superior oblique tendon is sandwiched between the superior rectus and the sclera. When the

FIGURE 11-20. Berk superior oblique tenotomy performed at the nasal tendon. (From Ref. 2, with permission.)

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temporal ﬁbers are removed from the sclera, they do not retract but, instead, scar down to sclera under the superior rectus muscle. Another disadvantage of the temporal tenotomy is that the tendon is extremely splayed out at its insertion; thus, it is difﬁcult to hook and tenotomize all the posterior superior oblique ﬁbers. The preferred procedure, developed by Marshall Parks, is to perform the superior oblique tenotomy nasal to the superior rectus muscle through a temporal conjunctival incision. By placing the conjunctival incision temporal to the superior rectus muscle and reﬂecting the incision nasally, the surgeon can keep the nasal intermuscular septum intact and minimize scleral–tendon scarring. Intact nasal intermuscular septum is vital to maintain the anatomic relationship of the superior oblique tendon and helps reduce the incidence of postoperative superior oblique palsy.

Wright Superior Oblique Tendon Expander This procedure controls the separation of the ends of the tendon, allowing quantiﬁcation of tendon separation.16 A segment of a silicone 240 retinal band is inserted between the cut ends of the superior oblique tendon (Fig. 11-21). The length of silicone is determined by the degree of superior oblique overaction, as well as the amount of A-pattern and downshoot. The maximum length of silicone is 7 mm, but most signiﬁcant Brown’s syndromes can be surgically managed with a segment of 5 to 6 mm.17 Perform the superior oblique expander through a temporal conjunctival incision, even though the silicone is placed in the nasal tendon. By placing the conjunctival incision temporal to the superior rectus muscle, then reﬂecting the incision nasally, the surgeon can keep the nasal superior oblique tendon capsule ﬂoor and intermuscular septum intact and prevent adhesion of the silicone implant to sclera. This maneuver is analogous to cataract surgery and placing an intraocular lens (IOL) in the capsular bag. An intact nasal tendon capsule ﬂoor is important to maintain the anatomic relationships of the superior

FIGURE 11-21A,B. Wright superior oblique tendon expander. (A) A segment of 240 silicone retinal band is sutured between the cut ends of the superior oblique tendon. (B) The silicone segment elongates the tendon.

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oblique tendon insertion and not create a new insertion site nasal to the superior rectus muscle. Scarring of the silicone to nasal sclera or the nasal aspect of the superior rectus muscle can cause limitation of depression postoperatively.

SLIPPED OR LOST RECTUS MUSCLE An important complication of strabismus surgery is a slipped or lost muscle. The medial rectus muscle is the muscle most commonly lost or slipped after strabismus surgery and is the most difﬁcult to retrieve, as there are no fascial connections to oblique muscles that keep the muscle from retracting posteriorly. In contrast, the inferior, superior, and the lateral recti have check ligaments that connect to adjacent oblique muscles. A slipped rectus muscle occurs when a muscle retracts posterior to the intended recession or resection point but there is some tissue still attached to the intended scleral insertion. A slipped muscle after strabismus surgery is caused by inadvertently suturing the muscle capsule or anterior Tenon’s capsule instead of true muscle tendon. Anterior Tenon’s capsule and muscle capsule are then secured to sclera, so the muscle slips posteriorly while a “pseudotendon” of connective tissue remains attached to sclera. A lost muscle occurs when the muscle retracts posteriorly and there is no connection of the muscle to sclera. Orbital trauma or hemorrhage can also result in a lost or damaged muscle.3 Typical signs of a slipped or lost muscle include decreased muscle function with limited ductions and lid ﬁssure widening in the ﬁeld of action of the lost muscle. On occasion, the presentation may be subtle, with slight limitation of ductions as the only ﬁnding. The key observation is an incomitant deviation with underaction of the slipped muscle. Initial eye alignment during the ﬁrst postoperative week may be fairly good in primary position, with only a mild limitation of ductions. Over several weeks to months, however, ductions become progressively more limited. This progression probably represents muscle slippage in addition to secondary contracture of the antagonist muscle against a weakened slipped muscle. Management of a slipped or lost muscle is to ﬁnd the muscle and surgically advance it to anterior sclera if possible. Fullthickness locking bites through muscle ﬁbers must be obtained, because partial-thickness locking bites may result in slippage of

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the posterior tendon ﬁbers. If a lost muscle cannot be retrieved, then a transposition procedure, such as the Hummelsheim, should be performed.

STRETCHED INSERTION SCAR In contrast to a slipped or lost muscle that results in an immediate overcorrection, there are many cases where an overcorrection occurs 4 to 6 weeks, and some-times years, after muscle surgery (Fig. 11-22). When this overcorrection is associated with minimal underaction of the operated muscle, consider a stretched or elongated scar, with the operated muscle migrating posteriorly. Late overcorrection is particularly common after inferior rectus recession for a hypotropia associated with thyroid disease, as it occurs in approximately 50% of cases.12 There has been much speculation about the cause for this late overcorrection,15 but work by Ludwig probably provides the best explanation.9,10 This theory states that the new insertion scar of the muscle to sclera stretches after the suture dissolves. The 6-0 vicryl suture used by most ophthalmologists lasts about 3 to 6 weeks, thus explaining the timing of the overcorrection. In this author’s (K.W.W.) experience, the use of a nonabsorbable suture reduces the problem of late overcorrection of the inferior rectus muscle. Any rectus muscle can have a stretched scar and a late overcorrection including, in order of frequency, inferior rectus, medial rectus, and superior rectus muscles. The likelihood of stretched scar formation may be inversely related to the length of the muscle’s arc of contact.4

BOTULINUM NEUROTOXIN Botulinum is a cholinergic blocking agent. Blockage in a muscle occurs by binding sodium at the myoneural junction, causing the loss of acetylcholine activity that paralyzes the muscle. Minimal diffusion occurs through the nerve or the muscle because there is tight binding within the muscle. Injection of botulinum toxin into a rectus muscle results in paralysis that occurs after 24 to 48 h and lasts from 3 to 6 months. The most common strabismus indication for use of botulinum is sixth nerve palsy. The treatment is to inject the ipsi-

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FIGURE 11-22A,B. Late overcorrection (4 weeks after strabismus surgery) after a left inferior rectus recession for thyroid-related, tight inferior rectus muscle. The left inferior rectus muscle was found to be posterior, caused by a stretched scar. (A) Note the left hypertropia and lower lid retraction. (B) Limited depression, left eye.

lateral medial rectus muscle (antagonist of the paretic lateral rectus muscle). The induced weakness of the medial rectus muscle from botulinum injection balances forces against the weak lateral rectus muscle (weakness with weakness), which

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theoretically allows the paretic muscle to regain its strength without secondary contracture of the antagonist. The use of botulinum is controversial, as studies have not shown an improvement in recovery rates for sixth nerve palsy (see Chapter 10). Botulinum has also been used for comitant strabismus. The rationale for using botulinum toxin in nonparalytic strabismus is twofold: to weaken and lengthen the injected muscle and to induce a mild secondary contracture in the injected muscle’s antagonist. Botulinum causes secondary muscle contracture by paralyzing the injected muscle, producing a large consecutive deviation in the opposite direction; this causes shortening and contracture of the antagonist to the injected muscle, theoretically leading to a permanent correction of the strabismus even after the botulinum wears off. In infantile strabismus, it is theorized that the overacting muscle can be injected before the development of contracture. Because of the temporary large overcorrection associated with the initial paralysis and the need for multiple injections to correct strabismus, strabismus surgery is usually preferred for the treatment of comitant strabismus.

References 1. Apt L, Call NB. Inferior oblique muscle recession. Am J Ophthalmol 1978;95:95–100. 1a. Beisner DH. Reduction of ocular torque by medial rectus recession. Arch Ophthalmol 1971;85:13. 2. Berk RN. Tenotomy of the superior oblique for hypertropia. Arch Ophthalmol 1947;38:605. 3. Cates CA, et al. Slipped medial rectus muscle secondary to orbital hemorrhage following strabismus surgery. J Pediatr Ophthalmol Strabismus 2000;37:361–362. 4. Chatzistefanou KI, et al. Magnetic resonance imaging of the arc of contact of extraocular muscles: implications regarding the incidence of slipped muscles. J Am Assoc Pediatr Ophthalmol Strabismus 2000; 4:84–93. 4a. Elliot L, Nankin J. Anterior transposition of the inferior oblique. J Pediatr Ophthalmol Strabismus 1981;18:35. 5. Eustis HS, Leoni R. Early reoperation after vertical rectus muscle surgery. J Am Assoc Pediatr Ophthalmol Strabismus 2001;5:217–220. 6. Guemes A, Wright KW. Effect of graded anterior transposition of the inferior oblique muscle on versions and vertical deviation in primary position. J Am Assoc Pediatr Ophthalmol Strabismus 1998;2;201– 206. 7. Kushner BJ. Fifteen-year outcome of surgery for the near angle in patients with accommodative esotropia and a high accommodative

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convergence to accommodation ratio. Arch Ophthalmol 2001;119: 1150–1153. 8. Kushner BJ, et al. Should recessions of the medial recti be graded from the limbus or the insertion? Arch Ophthalmol 1989;107:1755– 1758. 9. Ludwig IH. Scar remodeling after strabismus surgery. Trans Am Ophthalmol Soc 1999;97:583–651. 10. Ludwig IH, Chow AY. Scar remodeling after strabismus surgery. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4:326–333. 10a. Mims JL, Wood RC. Bilateral anterior transposition of the inferior obliques. Arch Ophthalmol 1989;107:41. 11. Recchia FM, et al. Endophthalmitis after pediatric strabismus surgery. Arch Ophthalmol 2000;118:939–944. 12. Sprunger DT, Helveston EM. Progressive overcorrection after inferior rectus recession. J Pediatr Ophthalmol Strabismus 1993;30:145– 148. 12a. Stager DR. The neuroﬁbrovascular bundle of the inferior oblique muscle as its ancillary origin. Trans Am Ophthalmol Soc 1996;94: 1073–1094. 13. Wright KW. Brown’s syndrome: Diagnosis and management. Trans Am Ophthalmol Soc 1999;XCVII:1023–1109. 14. Wright KW. Color atlas of ophthalmic surgery: strabismus. Philadelphia: Lippincott, 1991:173–193. 15. Wright KW. Late overcorrection after inferior rectus recession. Ophthalmology 1996;103:1503–1507. 16. Wright KW. Superior oblique silicone expander for Brown’s syndrome and superior oblique overaction. J Pediatr Ophthalmol Strabismus 1991;28(2):101–107. 17. Wright KW. Surgical procedure for lengthening the superior oblique tendon. Investig Ophthalmol Vis Sci 1989;30(suppl):377. 18. Wright KW, Lanier AB. Effect of a modiﬁed rectus tuck on anterior segment circulation in monkeys. J Pediatr Ophthalmol Strabismus 1991;28:77–81. 19. Wright KW, Min BM, Park C. Comparison of superior oblique tendon expander to superior oblique tenotomy for the management of superior oblique overaction and Brown’s syndrome. J Pediatr Ophthalmol Strabismus 1992;29(2):92–97; discussion 98–99.

12 Ocular Motility Disorders Mitra Maybodi, Richard W. Hertle, and Brian N. Bachynski

N

ormal individuals and most patients with common concomitant childhood strabismus have full ocular rotations (versions and ductions). This chapter is devoted to some of the more frequently encountered childhood disorders of the central and peripheral nervous systems, neuromuscular junction, and extraocular muscles that appear clinically to have incomitant ocular misalignments. Analysis of ocular alignment, versions, ductions, forced ductions, and generated force allows the examiner to sort the causes of these limited eye movements into three general categories: (1) neuromuscular dysfunction, (2) restriction of the globe by orbital tissues, and (3) combined neuromuscular dysfunction and restriction (Fig. 12-1). Diagnosis in children is especially challenging because it is rarely possible to clinically test the force generated by extraocular muscle action. A general anesthetic is routinely required to perform forced ductions. It may therefore be necessary to base diagnostic and therapeutic decisions on incomplete clinical information, and the clinician must rely on familiarity with the epidemiologic and clinical characteristics of each disorder.

DISORDERS OF THE CENTRAL AND PERIPHERAL NERVOUS SYSTEMS Eye movement disorders arising from disturbance of the normal neurophysiology may be classiﬁed as supranuclear, internuclear, or infranuclear. 423

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FIGURE 12-1. Clinical evaluation of range of eye movements. Versions and cover test measurements allow the examiner to decide whether the eye movements are normal (no limitation) or limited. Forced duction testing is used to differentiate a restriction (positive resistance to movement of the globe) from a “paresis” (no resistance to movement of the globe).

Supranuclear Eye Movements Cranial nerves III, IV, and VI serve together with the extraocular muscles as a ﬁnal mechanism that executes all eye movements. Supranuclear pathways initiate, control, and coordinate various types of eye movements. Several types of eye movements are brieﬂy mentioned here (Table 12-1), but a detailed and lucid synthesis of current concepts of the neural control of eye movements can be found in many other sources.288

PHYSIOLOGY AND CLINICAL ASSESSMENT The vestibular apparatus drives reﬂex eye movements, which allow us to keep images of the world steady on the retinas as we move our heads during various activities. The eyes move in the opposite direction to the movement of the head so that they remain in a steady position in space. The semicircular canals are the end organs that provide the innervation to the vestibular

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nuclei, which in turn drive cranial nerves III, IV, and VI to compensate for rotations of the head. In contrast, the otoliths respond to linear accelerations of the head and to gravity when the head is tilted. You can easily test the effectiveness of input from the semicircular canals by testing the vestibulo-ocular reﬂex (VOR). First, hold your head still and observe an object such as your index ﬁnger as you move it side to side at about 1 to 3 cycles/s. The image is a blur. However, if you hold your ﬁnger steady and rotate your head from side to side at the same frequency, you are able to maintain a clear image. Several forms of saccades, fast eye movements, can be clinically observed. Voluntary saccades may be predictive, in anticipation of a target appearing in a speciﬁc location; command-generated, in response to a command such as “look to the right”; memory-guided; or antisaccades, in which a reﬂexive saccade to an abruptly appearing peripheral target is suppressed and, instead, a voluntary saccade is generated in the equidistant but opposite direction. Involuntary saccades consist of the fast phase of nystagmus due to vestibular and optokinetic stimuli; spontaneous saccades, providing repetitive scanning of the environment, although also occurring in the dark and in severely visually impaired children; and reﬂex saccades, occurring involuntarily in response to new visual, auditory, olfactory, or tactile cues, suppressable by antisaccades.83

TABLE 12-1. Types of Eye Movements. Type of eye movement

Function

Stimulus

Clinical tests

Vestibular

Maintain steady ﬁxation during head rotation

Head rotation

Fixate on object while moving head; calorics

Saccades

Rapid reﬁxation to eccentric stimuli

Eccentric retinal image

Voluntary movement between two objects; fast phases of OKN or vestibular nystagmus

Smooth pursuit

Keep moving object on fovea

Retinal image slip

Voluntarily follow a moving target; OKN slow phases

Vergence

Disconjugate, slow movement to maintain binocular vision

Binasal or bitemporal disparity; retinal blur

Fusional amplitudes; near point of convergence

OKN, optokinetic nystagmus.

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The pathway of saccades originates in the visual cortex and projects through the anterior limb of the internal capsule, through the diencephalon. It then divides into dorsal and ventral pathways, the dorsal limb going to the superior colliculi, and the ventral limb (which contains the ocular motor pathways for horizontal and vertical eye movements) to the pons and midbrain. The superior colliculus acts as an important relay for some of these projections (Fig. 12-2). The neurons responsible for generating the burst, or discharge, for saccades are classiﬁed as excitatory burst neurons (EBN); inhibitory burst neurons (IBN) function to silence activ-

FIGURE 12-2. The superior colliculi are a pair of ovoid masses composed of alternating layers of gray and white matter; they are centers for visual reﬂexes and ocular movements, and their connections to other structures in the brain and spinal cord are varied and complex. Some of these other structures include the retina, visual and nonvisual cerebral cortex, inferior colliculus, paramedian pontine reticular formation, thalamus, basal ganglia, and spinal cord ventral gray horn. The ﬁbers of the medial longitudinal fasciculus form a fringe on its ventrolateral side: 1, superior (cranial) colliculus; 2, brachium of superior (cranial) colliculus; 3, medial geniculate nucleus; 4, brachium of inferior (caudal) colliculus; 5, central gray substance; 6, cerebral aqueduct; 7, visceral nucleus of oculomotor nerve (Edinger–Westphal nucleus); 8, nucleus of oculomotor nerve; 9, medial lemniscus; 10, central tegmental tract; 11, medial longitudinal fasciculus; 12, red nucleus; 13, ﬁbers of oculomotor nerve; 14, substantia nigra; 15, basis pedunculi.

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FIGURE 12-3. Brainstem structures controlling eye movements. Parasagittal section of the cerebrum and brainstem shows areas of the ocular motor nuclei and brainstem structures involved with internuclear and supranuclear pathways. PC, posterior commissure; SC, superior colliculus; IC, inferior colliculus; Pi, pineal; riMLF, rostral interstitial nucleus of the medial longitudinal fasciculus; INC, interstitial nucleus of Cajal; CN III, IV, VI, cranial nerve III, IV, VI; MLF, medial longitudinal fasciculus; PPRF, paramedian pontine reticular formation; VN, vestibular nuclei.

ity in the antagonist muscle during the saccade. In the brainstem, the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) and the pontine paramedian reticular formation (PPRF) provide the saccadic velocity commands, by generating the “pulse of innervation” immediately before the eye movement, to cranial nerves III, IV, and VI. Horizontal saccades are generated by EBN in the PPRF, which is found just ventral and lateral to the MLF in the pons (Figs. 12-3, 12-4, 12-5), and by IBN in the nucleus paragigantocellularis dorsalis just caudal to the abducens nucleus in the dorsomedial portion of the rostral medulla. Vertical and torsional components of saccades are generated by EBN and IBN in the riMLF, located in the midbrain. Following a saccade, a “step of innervation” occurs during which a higher level of tonic innervation to ocular motoneurons keeps the eye in its new position, against orbital elastic forces

FIGURE 12-4. Transverse section of caudal pons. AbdNu, abducens nucleus; AbdNr, abducens nerve; AMV, anterior medullary velum; CSp, corticospinal tract; FacG, internal genu of facial nerve; FacNr, facial nerve; FacNu, facial nucleus; LVN, lateral vestibular nucleus; ML, medial lemniscus; MLF, medial longitudinal fasciculus; MVN, medial vestibular nucleus; RetF, paramedian pontine reticular formation; SCP, superior cerebellar peduncle; SpTNu, spinal trigeminal nucleus; SpTT, spinal trigeminal tract; SVN, superior vestibular nucleus. (Adapted from Haines DE. Neuroanatomy: an atlas of structures, sections, and systems. Baltimore: Urban & Schwarzenberg, 1983, with permission.)

FIGURE 12-5. Schematic of brainstem pathways coordinating horizontal saccades. The PPRF, after receiving input from the ipsilateral cortical centers and superior colliculus, stimulates two sets of neurons in the abducens nucleus: (1) those that send axons to innervate the ipsilateral lateral rectus and (2) those whose axons join the MLF and subsequently activate the medial rectus subnuclei of the contralateral third nerve. PPRF, paramedian pontine reticular formation; VI, sixth cranial nerve nucleus; III, third cranial nerve nucleus.

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that would restore the eye to an anatomically “neutral” position. For horizontal saccades, the step of innervation comes from the neural integrator (see following), primarily from the nucleus prepositus–medial vestibular nucleus complex. The eye is held steady at the end of vertical and torsional saccades by the step of innervation provided from the interstitial nucleus of Cajal in the midbrain.288 In addition to burst neurons, omnipause neurons, located in the nucleus raphe interpositus in the midline of the pons, between the rootlets of the abducens nerves, are essential for normal saccadic activity. Continuous discharge from omnipause neurons inhibits burst neurons, and this discharge only ceases immediately before and during saccades.288 Other burst neurons termed long-lead burst neurons (LLBN) have also been identiﬁed that discharge 40 ms before saccades, whereas the previously mentioned burst cells discharge 12 ms before saccades. Some LLBN lie in the midbrain, receiving projections from the superior colliculus and projecting to the pontine EBN, medullary IBN, and omnipause neurons. Other LLBN lie in the nucleus reticularis tegmenti pontis (NRTP), projecting mainly to the cerebellum but also to the PPRF. It appears that LLBN receiving input from the superior colliculus may play a crucial role in transforming spatially coded to temporally coded commands, whereas other LLBN may synchronize the onset and end of saccades.288 If an abnormality of saccadic eye movements is suspected, the quick phases of vestibular and optokinetic nystagmus (OKN) can be easily evaluated in infants and young children. To produce and observe vestibular nystagmus, hold the infant at arm’s length, maintain eye contact, and spin ﬁrst in one direction and then in the other. An OKN response can be elicited in the usual manner by passing a repetitive stimulus, such as stripes or an OKN drum, in front of the baby ﬁrst in one direction and then in another. In addition, reﬂex saccades are induced in many young patients when toys or other interesting stimuli are introduced into the visual ﬁeld. Older children are asked to ﬁxate alternately upon two targets so that the examiner can closely observe the saccades for promptness of initiation, speed, and accuracy. Smooth pursuit permits us to maintain a steady image of a moving object on our foveas and thereby to track moving targets with clear vision. The pathways for smooth pursuit have not been fully elucidated, but it appears that frontal and extrastriate

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visual cortex transmits information about the motion of both the target and the eyes to the dorsolateral pontine nuclei (DLPN). This complex signal travels from the DLPN to the cerebellum (paraﬂocculus, ﬂocculus, and dorsal vermis), and from the cerebellum via the vestibular and fastigial nuclei to its ﬁnal destination, the ocular motor nerve nuclei III, IV, and VI. Unilateral lesions in the cortex and cerebellum affect smooth pursuit toward the side of the lesion. Vergences are eye movements that turn the eyes in opposite directions so that images of objects will fall on corresponding retinal points. Two major stimuli are known to elicit vergences: (1) retinal disparity, which leads to fusional vergences, and (2) retinal blur, which evokes accommodative vergences. Convergence of the eyes, accommodation of the lens, and constriction of the pupils occur simultaneously when there is a shift in ﬁxation from distance to near; together, these actions constitute the near triad. The neural substrate for vergence lies in the mesencephalic reticular formation, dorsolateral to the oculomotor nucleus. Neurons in this region discharge in relation to vergence angle (vergence tonic cells), to vergence velocity (vergence burst cells), or to both vergence angle and velocity (vergence burst-tonic cells). Although most of these neurons also discharge with accommodation, experiments have shown that some do remain predominantly related to vergence.32 Like versional movements, a velocity-to-position integration of vergence signals is necessary. The nucleus reticularis tegmenti pontis (NRTP) has been shown to be important in the neural integration, that is, velocity-to-position integration, of vergence signals. The cells in NRTP that mediate the near response appear to be separate from the cells which mediate the far response. Lesions of NRTP cause inability to hold a steady vergence angle. NRTP has reciprocal connection with the cerebellum (nucleus interpositus) and receives descending projections from several cortical and subcortical structures.32,288 The cerebellum plays an important role in eye movements. Together with several brainstem structures, including the nucleus prepositus and the medial vestibular nucleus, it appears to convert velocity signals to position signals for all conjugate eye movements through mathematical integration. Because of this, all the structures involved in this process are often referred to as the neural integrator. The role of the neural integrator in horizontal saccades was mentioned earlier.

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To test the neural integrator clinically, observe ﬁxation, ﬁxation in eccentric gaze, saccades, pursuit, and OKN and also test for rebound nystagmus and VOR cancellation. To examine for rebound nystagmus, ﬁrst ask the patient to ﬁxate on a target from the primary position, then to reﬁxate on an eccentric target for 30 s, and ﬁnally to return to the original primary position target. A patient with rebound nystagmus will show transient nystagmus with the slow phases toward the previous gaze position. To evaluate a child’s VOR cancellation, it is easiest to place your hand on top of the patient’s head to control both the head and a ﬁxation target that will extend in front of the child’s visual axis. You may use a Prince rule with a picture attached. Ask the child to ﬁxate on the target as you passively rotate both the head and the target side to side. If the child is unable to cancel the VOR, you will observe nystagmus instead of the steady ﬁxation expected in normal subjects. Patients with faulty neural integration may show gazeevoked nystagmus, impaired smooth pursuit, inability to cancel the vestibulo-ocular reﬂex during ﬁxation, saccadic dysmetria, defective OKN response, or rebound nystagmus. Most frequently, gaze-evoked nystagmus is seen in conjunction with use of anticonvulsants or sedatives. However, because 60% to 70% of brain tumors in children are subtentorial, acquired eye movement abnormalities suggesting defective neural integration, whether isolated or associated with other neurological deﬁcits, alert the examiner to investigate for a serious central nervous system abnormality.39,110,132 Structural anomalies affecting the brainstem and cerebellum, for example, the Arnold–Chiari malformation, as well as metabolic, vascular, and neurodegenerative disorders, may also produce abnormalities of the neural integrator. Reﬂex eye movements such as the vestibulo-ocular reﬂex and Bell’s phenomenon are easy to elicit clinically and are very useful for gross localization of neural lesions. When both saccades and smooth pursuit in a certain direction are limited, the examiner tries to stimulate eye movements in that same direction with a doll’s head (oculocephalic) maneuver, spin test, or forced lid closure. If any of the reﬂex eye movements are intact, the appropriate cranial nerve(s) and extraocular muscles(s) are clearly functioning, and the defect is necessarily supranuclear.

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DISORDERS OF SUPRANUCLEAR EYE MOVEMENTS We focus here on a few disorders in which the normal physiology of supranuclear eye movements, such as saccade, smooth pursuit, vergence, and gaze holding, is disturbed.

SACCADE INITIATION FAILURE/OCULAR MOTOR APRAXIA The term saccade initiation failure or ocular motor apraxia is used to specify impaired voluntary saccades and variable deﬁcit of fast-phase saccades during vestibular or optokinetic nystagmus.380,447 Congenital ocular motor apraxia, ﬁrst described by Cogan,96 is a congenital disorder that is characterized by defective horizontal saccades, but it does not represent a true apraxia because reﬂex saccades may also be impaired. The incidence of this condition is dependent upon the underlying etiology. Etiology Patients with congenital saccade initiation failure show abnormal initiation and decreased amplitude of voluntary saccades; saccadic velocities in these patients are normal, and fast phases of nystagmus of large amplitude can occasionally be generated, suggesting that the brainstem burst neurons that generate saccades are intact.288 Acquired saccade initiation failure may be caused by any number of conditions, as listed in Table 122. Some of these patients with the acquired type, such as those with Gaucher’s disease (type 1 and some type 3 patients), do have abnormal saccadic velocities.83,194 Although the exact cause or localization of the defect in congenital saccade initiation failure has not been determined, there is strong evidence suggesting that most disorders that cause saccade initiation failure can be localized subtentorially, particularly to the cerebellar vermis.83,137,196,235,429,450 Clinical Features The clinical presentation varies with the age and motor development of the child. Infants and children with poor head control who are affected are commonly thought to be cortically blind because the expected visually driven eye movements are not observed.164,417 In such an infant, demonstration of vertical saccades, vertical pursuit, OKN response in any direction, or normal acuity on visual evoked response testing suggests the diagnosis of saccade initiation failure. However, lack of appropriate response to such testing does not exclude this diagnosis. Another suggestive clinical sign in young infants is an intermittent tonic deviation of the eyes in the direc-

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TABLE 12-2. Congenital and Acquired Saccade Initiation Failure (SIF) (Ocular Motor Apraxia). Classiﬁcation by cause Idiopathic195 Perinatal problems

Speciﬁc etiologies Cerebral palsy195; hypoxia195; hydrocephalus195; seizures195

Congenital malformations

Agenesis of corpus callosum450; fourth ventricle dilation and vermis hypoplasia450; Joubert’s syndrome282,332; macrocerebellum63; dysgenesis of cerebellar vermis and midbrain523; Dandy–Walker malformation195; immature development of putamen472; heterotropia of gray matter472; porencephalic cyst195,515; hamartoma near foramen of Munro515; macrocephaly195; microcephaly147,195; posterior fossa cysts375; chondrodystrophic dwarﬁsm and hydrocephalus98; encephalocele375; occipital meningocele11; COACH syndrome162 (cerebellar vermis hypoplasia, oligophrenia, congenital ataxia, coloboma, hepatic ﬁbrocirrhosis)

Neurodegenerative conditions with infantile onset of SIF

Infantile Gaucher’s disease (type 2, 3)85,100,507; Gaucher’s disease type 256,497; Pelizaeus–Merbacher disease195; Krabbe’s leukodystrophy195; proprionic academia195; GM1 gangliosidosis195; infantile Refsum’s disease195; 4hydroxybutyric aciduria147,397

Neurodegenerative conditions with later onset of SIF

Ataxia telangectasia473,499,532; spinocerebellar degenerations7,21,36,228,270,369,512; juvenile Gaucher’s disease (type 3)194; Huntington’s disease31,471; Hallervorden–Spatz disease17; Wilson’s disease265

Acquired disease

Postimmunization encephalopathy195,335; herpes encephalitis195; posterior fossa tumors195,298,477,536,540

Other associations

Alagille’s syndrome12; Bardet–Biedl syndrome284; carotid ﬁbromuscular hypoplasia195; Cockayne’s syndrome147; Cornelia de Lange syndrome195; juvenile nephronophthisis129; Lowe’s syndrome181; neuroﬁbromatosis type 1168; orofacial digital syndrome305; X-linked muscle atrophy with congenital contractures524

Source: Adapted from Cassidy L, Taylor D, Harris C. Abnormal supranuclear eye movements in the child: a practical guide to examination and interpretation. Surv Ophthalmol 2000;44:479–506, with permission.83

tion of slow-phase vestibular or optokinetic nystagmus; in these infants, fast-phase saccades may be impaired, again confounding our deﬁnition of oculomotor apraxia.288 Natural History With time, often by 4 to 8 months of age, the child develops a striking stereotypical “head-thrusting” behavior to reﬁxate. First, the eyelids blink (“synkinetic blink”)

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and the head begins to rotate toward the object of interest. Next, the head continues to rotate past the intended target, allowing the tonically deviated eyes, which are now in an extreme contraversive position, to come into alignment with the target. Finally, as the eyes maintain ﬁxation, the head rotates slowly back so that the eyes are in primary position. This apparent use of the VOR to reﬁxate continues for several years, but with increasing age, patients demonstrate less prominent head thrusting and may even be able to generate some saccades although these are abnormal.97,542 In some infants, generalized hypotonia may be associated. This hypotonia seems to be more pronounced in boys and improves with increasing age. These babies later demonstrate the motor delay, incoordination, and clumsiness that have been noted in the literature.153,395 Clinical Assessment The parents of children are asked about any associated developmental abnormality. A complete ophthalmic examination is performed to rule out any strabismus or amblyopia, as strabismus has been reported in 22% of these patients in one series.195 Vision, electroretinogram (ERG), and visual evoked potential (VEP) are normal in the congenital saccade initiation failure patients.164,451 Any coexistent abnormal vision, nystagmus, or abnormal ERG or VEP suggests associated disease.451 Neurological abnormalities or dysmorphic features are further investigated by the appropriate subspecialists. A brain MRI is necessary for any suspected neurological disorder, to look for any midline malformation, particularly around the fourth ventricle and cerebellar vermis.83 Systemic Associations Signiﬁcant structural abnormalities of the central nervous system (CNS) may be associated, such as lipoma477 or brainstem tumor.540 Joubert’s syndrome is associated with cerebellar hypoplasia and agenesis of the corpus callosum.282 A neuroradiologic correlation has been made in children with saccade initiation failure, in which 61% of 62 children had abnormal scans, primarily the brainstem and cerebellar vermis; however, signiﬁcant abnormalities in the cerebral cortex and basal ganglia were also found.450 Gaucher’s disease,185,197 ataxia telangiectasia7,473 and its variants, and Niemann–Pick variants100 may also present with the inability to generate saccades as well as blinking and head thrusting before reﬁxation. Unlike congenital saccade initiation

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failure, these disorders generally involve vertical as well as horizontal saccades and, of course, eventually manifest systemic signs. Early-onset vertical saccade initiation failure has been observed in children with lesions at the mesencephalic– diencephalic junction, presumably infarcts resulting from perinatal hypoxia.135,219 Inheritance Occasional familial occurrence,196,345,387,398,501 increased frequency in males, and occurrence in monozygotic twins67 suggest a genetic process in some cases. Association with nephronophthisis has been described in two patients, each of whom exhibited deletions on chromosome 2q13.55 Treatment No treatment is available for congenital saccade initiation failure, but associated strabismus is treated accordingly. Prognosis The visual and clinical prognosis of those patients with the congenital type is good. Many can adapt over time to allow gaze shifts with less head thrusting and can even generate some saccades, albeit still abnormal.97,542

INDUCED CONVERGENCE RETRACTION/PARINAUD DORSAL MIDBRAIN SYNDROME

OR

Lesions of the posterior commissure in the dorsal rostral midbrain (see Fig. 12-2) may result from many disease processes and can affect a variety of supranuclear mechanisms, including those that control vertical gaze, eyelids, vergence, ﬁxation, and pupils. Other terms such as pretectal syndrome, Koerber–Salus– Elschnig syndrome, Sylvian aqueduct syndrome, posterior commissural syndrome, and collicular plate syndrome all refer to this condition. Incidence A report of 206 patients with pretectal syndrome in one neurologist’s practice at a general hospital in southern California indicated the incidence to be 2.3% of all patients examined by this neurologist in an 18-year period.255 Of these 206 patients, 71 exhibited induced convergence retraction. Etiology and Systemic Associations The pretectum was conﬁrmed as the critical structure that is affected in this disorder, investigated clinicopathologically in humans91 and experimentally in monkeys.371,372 Also, isolated interruption of the

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TABLE 12-3. Causes of Childhood Dorsal Midbrain Syndrome. Classiﬁcation by cause

Speciﬁc etiologies

Tumor

Pineal germinoma, teratoma and glioma; pineoblastoma; others386

Hydrocephalus

Aqueductal stenosis with secondary dilation of third ventricle and aqueduct, or with secondary suprapineal recess compressing posterior commissure,89,366 commonly caused by cysticercosis in endemic areas

Metabolic disease

Gaucher100,492; Tay–Sach; Niemann–Pick154; kernicterus214; Wilson’s disease265; others

Midbrain/thalamic damage

Hemorrhage; infarction

Drugs

Barbiturates138; carbamazepine; neuroleptics

Miscellaneous

Benign transient vertical eye disturbance in infancy; trauma; neurosurgery445; hypoxia; encephalitis; tuberculoma; aneurysm102; multiple sclerosis

posterior commissure in humans produces the entire syndrome of upward gaze palsy, pupillary light–near dissociation, lid retraction, induced convergence retraction, skew deviation, and upbeat nystagmus.251 Among the many underlying causes of this condition are hydrocephalus, stroke, and pinealomas. Table 123 lists other reported etiologies and systemic associations. Clinical Features and Assessment The constellation of deﬁcits are (1) vertical gaze palsy, (2) light–near dissociation of the pupils, (3) eyelid retraction (Collier’s sign), (4) disturbance of vergence, (5) ﬁxation instability, and (6) skew deviation. Limitation of upward saccades is the most reliable sign of the convergence retraction. Upward pursuit, Bell’s phenomenon, and the fast phases of vestibular and optokinetic nystagmus may also be affected either at presentation or with progression of the underlying process. It is rare for upgaze to be unaffected. Pathological lid retraction and lid lag are also common (Collier’s sign). When the patient attempts upward saccades, a striking phenomenon, convergence and globe retraction, frequently occurs; this is not true nystagmus, despite the common description of this clinical ﬁnding as convergence-retraction nystagmus, because there is no true slow phase. This action is best elicited with down-moving OKN targets because each fast phase is replaced by a convergence-retraction movement. Cocontraction of the extraocular muscles has been documented during this convergence-retraction jerk.161

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Unlike the pathways from upward saccades, the pathways for downward saccades do not appear to pass through the posterior commissure (Figs. 12-3, 12-6). Perhaps because of this, disturbances of downgaze are not as predictable or uniform. Usually down-going saccades and pursuit are present, but they may be slow. Sometimes, especially in infants and children, there is a tonic downward deviation of the eyes that has been designated the “setting sun” sign, and down-beating nystagmus may also be observed. The “setting sun” sign may also be seen in children with hydrocephalus. Convergence spasm may occur during horizontal saccades and produce a “pseudoabducens palsy” because the abducting eye moves more slowly than the adducting eye.113 This phenomenon can cause reading difﬁculties early in the course of dorsal midbrain syndrome because it provides an obstacle to reﬁxation toward the beginning of a new line of text. Indeed, older children may present with numerous pairs of corrective

FIGURE 12-6A,B. Schematic of brainstem pathways coordinating downward (A) and upward (B) saccades. (A) Downward saccades. The PPRF activates neurons in the riMLF that send ﬁbers caudally to synapse upon the inferior rectus subnucleus of the ipsilateral third nerve and the contralateral superior oblique nucleus. Not shown in this diagram, ﬁbers from the contralateral PPRF carry corresponding signals simultaneously. (B) Upward saccades. The PPRF activates neurons in the riMLF that send ﬁbers through the posterior commisure to the superior rectus subnucleus of the contralateral third nerve and ﬁbers to the inferior oblique subnucleus of the ipsilateral third nerve. Not shown in this diagram, ﬁbers from the contralateral PPRF carry corresponding signals simultaneously. riMLF, rostral interstitial nucleus of the medial longitudinal fasciculus; INC, interstitial nucleus of Cajal; III, third cranial nerve nucleus; IV, fourth cranial nerve nucleus; PPRF, paramedian pontine reticular formation.

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spectacles that have been prescribed due to their “vague” complaints about reading and other near work. In other patients complaining of difﬁculties with near vision, convergence may be paralyzed. “Tectal” pupils are usually large and react more poorly to light than to near, and anisocoria is not uncommon. All children with convergence retraction deserve thorough, prompt neurological and neuroradiologic evaluation because timely intervention may be decisive. The natural history of this disorder is dependent on the underlying etiology. Treatment The underlying medical cause requires investigation and primary treatment. Once the condition is stable for a period of time, from 3 to 12 months, surgery has been performed with some success. In addition to treating the coexistent diplopia from skew deviation or horizontal strabismus, which may be surgically corrected, the anomalous head posture from defective vertical gaze may also be treated by inferior rectus recession or vertical transposition of horizontal recti during simultaneous horizontal strabismus correction.74 Faden operation (posterior ﬁxation suture, or retroequatorial myopexy) on both medial recti to control convergence spasms and bilateral superior rectus resection to alleviate the anomalous head posture have also been reported.465 Prognosis The medical prognosis is dependent upon the underlying etiology. In the aforementioned review of 206 patients, only 20 patients died: 11 of tumors, 7 after strokes, and 1 with transtentorial hernation with tuberculous abscess. The good prognosis in this series may have been skewed by the preponderance of patients with cysticercal hydrocephalus.255 The prognosis of strabismus surgery in all eviating anomalous head posture and diplopia was good in all three patients in one study after a minimum of 6 months follow-up.74 In another report, head posture and ocular motility improved beyond expectation and remained satisfactory after a minimum of 1 year follow-up.465

TRANSIENT VERTICAL GAZE DISTURBANCES

IN INFANCY

Vertical gaze abnormalities may be benign and transient in infants. Four babies with episodic conjugate upgaze that became less frequent over time have been described.6,113 During these episodes, normal horizontal and vertical vestibulo-ocular responses could be observed.

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Tonic downgaze has been observed in 5 of 242 consecutively examined healthy newborn infants215 as well as in other infants.113,285 Again, the eyes can easily be driven above the primary position with the vestibulo-ocular reﬂex. Also, the eyes show normal upward movements during sleep. In contrast, infants with hydrocephalus who manifest the “setting sun” sign do not elevate the eyes during sleep or with an oculocephalic maneuver. Premature infants with intraventricular hemorrhage may also develop tonic downgaze, usually in association with a largeangle esotropia.480 These infants do not elevate the eyes with vestibular stimulation. Upgaze often returns during the ﬁrst 2 years of life, but the esotropia does not resolve when upgaze returns.

DOUBLE ELEVATOR PALSY/MONOCULAR ELEVATION DEFICIENCY Monocular deﬁciency of elevation, that is, an apparent weakness of both the superior rectus and inferior oblique muscles, has been termed double elevator palsy or monocular elevation deﬁciency. This deﬁcit may be caused by mechanical restriction of the globe or neural dysfunction at the supranuclear, nuclear, or infranuclear level. Congenital double elevator palsy of supranuclear origin is conﬁrmed on clinical examination if the affected eye elevates during Bell’s phenomenon or doll’s head maneuver.44,52

SPASM

OF THE

NEAR REFLEX

Spasm of the near reﬂex, also referred to as convergence spasm, is characterized by intermittent spasm of convergence, of miosis, and of accommodation.95 Symptoms include headache, photophobia, eyestrain, blurred vision, and diplopia. Patients may appear to have bilateral sixth nerve palsies, but careful observation will reveal miosis and high myopia (8–10 D) on dry retinoscopy, accompanying the failure of abduction.172 This key clinical clue prevents misdiagnosis and misdirected testing.172,182,252,430 Most commonly, spasm of the near reﬂex is psychogenic, and treatment may include simple reassurance, psychiatric counseling, or cycloplegia with bifocals. However, a number of cases of spasm of the near reﬂex associated with organic disease have been reported.487 In a series of seven patients, two had

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posterior fossa abnormalities (cerebellar tumor, Arnold–Chiari malformation), two had pituitary tumors, one had a vestibulopathy, and two had antecedent trauma.112 None of these patients appeared to have a personality disorder, and none complained of signiﬁcant disability. Nevertheless, no clear causal relationship or uniﬁed neuroanatomic localization has been established. It is prudent to keep in mind that just as any patient with organic disease may also have a functional disorder, disturbances that are clearly functional do not exclude coexisting organic disease.

Internuclear Opththalmoplegia In the absence of peripheral lesions such as myasthenia gravis, failure of adduction combined with nystagmus of the contralateral abducting eye is termed internuclear ophthalmoplegia (INO) and localizes the lesion to the medial longitudinal fasciculus (MLF) unequivocally.

ETIOLOGY The abducens nucleus consists of two populations of neurons that coordinate horizontal eye movements (see Fig. 12-5). Fibers from one group form the sixth nerve itself and innervate the ipsilateral lateral rectus muscle; ﬁbers from the second group join the contralateral MLF and project to the subnucleus of the third nerve, which supplies the contralateral medial rectus muscle. In this way, the neurons of the sixth nerve nucleus yoke the lateral rectus with the contralateral medial rectus.

CLINICAL FEATURES Clearly, lesions of the abducens nucleus will cause an ipsilateral conjugate gaze palsy. Lesions of the MLF between the midpons and oculomotor nucleus, in turn, disconnect the ipsilateral medial rectus subnucleus from the contralateral sixth nerve nucleus and cause diminished adduction of the ipsilateral eye on attempted versions (see Fig. 12-3). The signs of INO may be accompanied by an ipsilateral hypertropia or skew deviation.

CLINICAL ASSESSMENT A subtle adduction deﬁcit is best appreciated when repetitive saccades are attempted; the adducting eye will demonstrate a slow, gliding, hypometric movement in conjunction with overshoot of the abducting eye. Usually, the ipsilateral eye can be

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adducted with convergence, but convergence will also be impaired if the MLF lesion is rostral enough to involve the medial rectus subnucleus.

SYSTEMIC ASSOCIATIONS Similar to dorsal midbrain syndrome, INO is an anatomic rather than etiological diagnosis. A host of structural, metabolic, immunological, inﬂammatory, degenerative, and other processes can interfere with the function of the MLF and nearby structures. In young adults, multiple sclerosis is by far the most common cause of INO.342 Multiple sclerosis also underlies most cases of bilateral INO. Although patients with bilateral INO generally remain orthotropic in primary position, they sometimes exhibit an exotropia in the wall-eyed bilateral internuclear ophthalmoplegia (WEBINO) syndrome.311 Additional causes of INO include Arnold–Chiari malformation,23,99,118,533 hydrocephalus,352 meningoencephalitis,64,226 brainstem or fourth ventricular tumors,99,439,482,496 head trauma,49,84,254 metabolic disorders, drug intoxications, paraneoplastic effect, carcinomatous meningitis, and others. Peripheral processes, particularly myasthenia gravis and Miller Fisher syndrome, may closely mimic INO and should be considered in any patient with INO-like eye movements.

TREATMENT AND PROGNOSIS The ﬁrst goal is to treat the underlying etiology. For example, steroid therapy is necessary in multiple sclerosis, and blood pressure management is required for a hypertensive stroke. After this initial consideration, if the disorder persists and remains stable for at least 6 months, the accompanying exotropia may be corrected by surgery. In a series of three patients treated surgically for diplopia caused by bilateral INO (from brainstem vascular disease) with exotropia of 55 to 70 prism diopters, favorable results were achieved by bilateral medial rectus resections and bilateral lateral rectus recessions (with one lateral rectus on an adjustable suture in each of the three).74 After a minimum of 6 months postoperative follow-up, all three patients achieved excellent cosmesis. In one of the three patients, binocularity was restored in the primary position, in the second diplopia was eliminated in primary and downgaze, and in the third diplopia was completely eliminated.

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Ocular Motor Cranial Nerve Palsies The processes that produce ocular motor nerve palsies in infants and children, as many neurological diseases in this age group, are commonly diffuse.

GENERAL CLINICAL CONSIDERATIONS Muscle paralysis is diagnosed by the inability of the eye to move in the direction of action of the particular muscle voluntarily and reﬂexively, tested by the doll’s head maneuver, spin test (looking for vestibular nystagmus), or forced lid closure (looking for Bell’s phenomenon). Paresis of a muscle may be detected on testing of versions, at which time version in a particular direction may be limited but ductions may appear full. If the muscle is totally paralyzed, the ductions will be limited as well; in this case, if it is possible to perform a forced duction test, the test would reveal no restriction in the direction of action of a paretic muscle. However, after long-standing muscle paresis, the muscle may become tightened, and forced duction testing in the direction opposite to that of the muscle action would reveal restriction. A subtle paresis is best appreciated when repetitive saccades are attempted; the eye will demonstrate a slow, gliding, hypometric movement in the direction of action of the particular muscle(s), in conjunction with overshoot of the other eye in that direction. The primary deviation, or the measured strabismus when ﬁxing with the normal eye, is smaller than the secondary deviation, which is the strabismus measured when ﬁxing with the restricted or paretic eye. Signiﬁcant factors in evaluating a child with ocular motor cranial palsies include (1) age of the child, (2) history of previous cranial nerve palsies or relevant systemic disease, (3) recent history of febrile illness, immunization, trauma, or exposure to toxins, (4) accompanying neurological symptoms or signs, and (5) the course under careful, regular observation. Any child exhibiting an ocular motor nerve palsy accompanied by other neurological signs deserves a consultation with a neurologist and a thorough, timely workup. It is incumbent upon the ophthalmologist to detect and treat any amblyopia that may occur. Also, prevention of amblyopia, by alternate patching, for example, can be considered in severely amblyogenic conditions such as third nerve palsies.

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The following discussion sets out an approach to the recognition and initial management of isolated third, fourth, and sixth nerve palsies and reviews some common childhood causes of combined ocular motor nerve palsies.

SIXTH NERVE PALSIES ETIOLOGY

AND

SYSTEMIC ASSOCIATIONS

Acquired sixth nerve palsies, whether isolated or not, are usually caused by tumors (especially glioma and medulloblastoma) and trauma (47%–62%).3,24,191,269,287,405 A signiﬁcant number of cases are also due to inﬂammatory causes such as meningitis (including from Lyme disease), Gradenigo’s syndrome,117 cerebellitis, and postviral sixth nerve palsy. The clinician is also faced with numerous other possible etiologies (Table 12-4).

CLINICAL FEATURES

AND

ASSESSMENT

As previously mentioned, a lesion affecting the sixth nerve nucleus produces an ipsilateral horizontal gaze palsy. Injury to the nerve at any other location along its course results in absent or poor abduction of the ipsilateral eye (Fig. 12-7). Of course, poor abduction is not speciﬁc to sixth nerve palsies and may also be caused by disorders of the neuromuscular junction (e.g., myasthenia gravis), restrictions (e.g., medial orbital wall fractures with tissue entrapment), and inﬂammation (e.g., orbital myositis). The examiner considers and excludes these possibilities before establishing the diagnosis of sixth nerve palsy. If a congenital anomaly of innervation, such as Duane’s syndrome, is clearly identiﬁed as the cause of abduction deﬁcit, no further investigation of the eye movement abnormality is necessary. Acute comitant esotropia can also follow head trauma (usually minor), febrile illness, migraine, or occlusion of an eye or may not be related to any obvious inciting cause.75,170,385,460 This condition is distinguishable on examination from a bilateral sixth nerve palsy. However, although an acute comitant esodeviation without accompanying signs is usually benign, it may in some cases be the harbinger of an intracranial tumor such as cerebellar astrocytoma or pontine glioma29,526 or other pathology such as a Chiari 1 malformation.517 Absence of symptoms or signs such as headaches, papilledema, or nystagmus may not rule out the possibility of an intracranial pathology. There-

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TABLE 12-4. Etiology of Infranuclear Sixth Nerve Palsy. Location/signs

Etiologies

Fascicle Ipsilateral VIIth nerve palsy, facial analgesia, loss of taste from anterior two thirds of tongue; peripheral deafness; Horner’s syndrome, contralateral hemiparesis

Tumor; demyelination; hemorrhage; infarction

Subarachnoid space Papilledema; other cranial nerve palsies

Meningitis; meningeal carcinomatosis; trauma; increased intracranial pressure causing downward pressure on brainstem; after lumbar puncture, shunt for hydrocephalus, spinal anesthesia, or halopelvic cervical traction; clivus tumor; cerebellopontine angle tumor; berry aneurysm; abducens neurinoma

Petrous apex Ipsilateral seventh nerve palsy; pain in eye or face; otitis media, leakage of blood or cerebrospinal ﬂuid from ear; mastoid ecchymosis; papilledema

Mastoiditis; thrombosis of inferior petrosal sinus; trauma with transverse fracture of temporal bone; persistent trigeminal artery, aneurysm, or arteriovenous malformation

Cavernous sinus/superior orbital ﬁssure Ipsilateral Horner’s syndrome; ipsilateral IIIrd, IVth, Vth cranial nerve involvement; proptosis; disc edema; orbital pain; conjunctival injection

Cavernous sinus thrombosis; carotid-cavernous ﬁstula; tumor; internal carotid aneurysm

Orbit Ipsilateral IIIrd, IVth, Vth cranial nerve involvement; proptosis; disc edema; orbital pain; conjunctival injection

Tumor; pseudotumor

Uncertain

Transient abducens palsy of newborn; after febrile illness or immunization; migraine; toxic; idiopathic

fore, a thorough ophthalmic examination is performed. MRI is indicated if the esotropia is unresponsive to correction of refractive error, there is no history of ﬂu-like illness, or no improvement is seen over the course of 1 to 4 weeks.

NATURAL HISTORY

AND

CLINICAL WORKUP

Newborns may demonstrate a transient sixth nerve palsy that is frequently unilateral and occasionally accompanied by a tem-

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FIGURE 12-7. Right sixth cranial nerve palsy. These photos show the limitation of abduction on attempted right gaze typical of a sixth cranial nerve palsy. Forced duction testing of this patient’s right eye showed no restriction to abduction.

porary ipsilateral seventh nerve palsy.53,267,291,400 Simple observation is generally sufﬁcient because resolution typically occurs within 4 to 10 weeks. Older infants and children may develop transient isolated sixth nerve palsies 1 to 3 weeks after nonspeciﬁc febrile or respiratory illnesses,267,405 after a speciﬁc viral illness such as varicella,350 after immunization,522 before mononucleosis,273 or without any obvious precipitating factor.435 Some of these palsies may recur, and the recurrences have no serious implications.2,60,65,399,474,476 Again, aggressive investigation is not warranted, but two simple studies are advised: (1) a complete blood count with differential, which may show lymphocytosis as evidence of a recent viral infection, and (2) examination of the ears for otitis media. The parents are warned to observe for any new signs or symptoms. Careful reexamination at regular intervals is essential; deterioration or improvement in lateral rectus function provide important evidence for or against a progressive mass lesion. Most children in this group recover abducens function within 10 weeks, although a prolonged (9 months) palsy may rarely occur.267 Persistence, without improvement, or deterioration of an isolated sixth nerve palsy in a child beyond about 3 months requires an intensive neurological, neuroradiologic, and otolaryngologic evaluation. In adults, a substantial number of isolated sixth nerve palsies that last beyond 6 months are caused by potentially treatable, often slow-growing, tumors.111,159,426 In a Mayo Clinic series of 133 children with acquired sixth nerve paresis, 15 presented with an isolated sixth nerve palsy due to tumor.405 Of these, 12

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developed additional neurological signs within a few weeks, whereas 3 patients took 2 to 3 months to develop additional signs. An additional problem is that a physician may not always be able to conﬁrm that the sixth nerve palsy in a child is isolated. Therefore, if close follow-up to resolution of the palsy or paresis is not possible, neuroimaging is recommended.24

TREATMENT Amblyopia prevention is always key in children younger than 7 to 9 years of age. Providing full hyperopic correction also relieves the demand for accommodation and thus decreases the chance of worsening esotropia. Treatment options include botulinus toxin injection and surgery. One approach is to inject botulinus toxin into the antagonist medial rectus muscle to prevent tightening of the unopposed medial rectus,442,444 sometimes allowing binocular vision in primary position, while the palsy is resolving.218 Reducing medial rectus contracture with botulinus toxin injection may also improve a surgical result.302

PROGNOSIS Spontaneous recovery of abduction in childhood sixth nerve palsy or paresis is much less common than in adults. The rate of residual strabismus was found to be 66% in one study of any sixth nerve palsy or paresis in patients 7 years of age and younger, likely a result of permanent structural deﬁcits without complete recovery in the setting of tumor and hydrocephalusshunt malfunction as the most frequent etiologies. The rate of amblyopia in this study was 20%, thus highlighting the need for parent education and close follow-up. The highest rates of spontaneous recovery have been reported in idiopathic (67%24), infectious (50%24), inﬂammatory (90%191), and traumatic (33%–50%24,191) cases.

FOURTH NERVE PALSY ETIOLOGY

AND

SYSTEMIC ASSOCIATIONS

Of the many causes of trochlear palsy in childhood (Table 12-5), “congenital” and traumatic are by far the most common.191,209 The cause of most congenital trochlear palsies remains unknown, but aplasia of the trochlear nucleus has been reported to accompany the absence of other cranial nerve nuclei.10,317,464 The superior oblique tendon or muscle is often the primary

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TABLE 12-5. Etiology of Fourth Nerve Palsy. Location/signs

Etiologies

Nucleus and fascicle Contralateral Horner’s syndrome

Trauma; tumor; demyelination; after neurosurgery; nuclear aplasia; arteriovenous malformation; hemorrhage; infarction

Subarachnoid space Papilledema; other cranial nerve palsies

Trauma; tumor; increased intracranial pressure; after lumbar puncture or shunt for hydrocephalus; spinal anesthesia; meningitis; mastoiditis

Cavernous sinus/superior orbital ﬁssure Ipsilateral Horner’s syndrome, ipsilateral IIIrd, Vth, VIth nerve involvement; proptosis; disc edema; orbital pain

Tumor; internal carotid aneurysm; Tolosa–Hunt syndrome

Orbit Ipsilateral IIIrd, VIth nerve involvement; proptosis; enophthalmos; disc edema; orbital pain; conjunctival/episcleral injection

Tumor; trauma; inﬂammation

Uncertain location

Congenital; idiopathic

problem. Laxity of this tendon has been described on forced duction testing381 and correlates well with the presence of attenuated superior oblique muscles on orbital MRI.432 Therefore, congenital cases may be more correctly termed congenital superior oblique palsy/underaction instead of fourth nerve palsy. Absence of the superior oblique muscle altogether is also in the differential of an apparent congenital superior oblique palsy.87 The trochlear nerves are particularly vulnerable to closed head trauma when there may be contrecoup of the tectum of the midbrain against the edge of the tentorium.292 In this way, the nucleus or fascicle may be injured within the substance of the midbrain, or the nerve itself may be contused as it exits the brainstem dorsally and passes laterally around the midbrain (see Fig. 123). The proximity of the two trochlear nerves to each other at the site of their crossing in the anterior medullary velum (roof of the Sylvian aqueduct; see Fig. 12-4) explains the high incidence of bilateral involvement after coup-contrecoup, closed head trauma.286

CLINICAL FEATURES

AND

ASSESSMENT

Vertical deviations may also result from other processes, such as abnormal neuromuscular transmission, restriction, inﬂam-

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mation, skew deviation, dissociated vertical divergence, small nonparalytic vertical deviations associated with horizontal strabismus, and paresis of other cyclovertical muscles. The clinical assessment of a vertical deviation is carefully executed to exclude these various possibilities. It is important to ask about previous extraocular muscle surgery or orbital trauma and to obtain any history that suggests myasthenia gravis or skew deviation. The examiner notes any anomalous head position (Figs. 12-8, 12-9), versions, ductions, cover test measurements in cardinal ﬁelds of gaze, any secondary deviation, forced (Bielschowsky) head tilt test measurements, presence or absence of both subjective and objective torsion, and presence or absence of dissociated vertical deviation. Forced ductions, Tensilon testing, and other supplemental tests are performed as appropriate.

A

B FIGURE 12-8. (A) Unilateral congenital cranial nerve palsy, right eye. The photograpph demonstrates a right hypertropia that increases in left gaze. There is slight underaction of the right superior oblique nad signiﬁcant overaction of the right inferior oblique muscle. (B) The photograph of head tilt test, with right hypertropia increasing on tilt right and diminishing on tilt left. Positive head tilt with the right hyper increasing in left gaze indicates a right superior oblique palsy.

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FIGURE 12-9. Bilateral asymmetric congenital fourth nerve palsy and esotropia. Note that the right superior oblique palsy is more severe than the left, and there is a right hypertropia in primary position. There is signiﬁcant superior oblique underaction, right side more than left side. A signiﬁcant V-pattern is present. There is a right hypertropia in right gaze and a left hypertropia in left gaze.

Several other comments regarding the clinical evaluation are crucial. 1. The familiar “Parks–Bielschowsky three-step” test helps to combine information from cover test measurements and the Bielschowsky head tilt phenomenon.59,370 This test is only useful when there is a palsy of a single cyclovertical muscle and can therefore only be applied after the careful assessment just described.281 A fourth nerve palsy would reveal hypertropia, worsening on horizontal gaze in the direction contralateral to the hypertropic eye, and worsening on head tilt ipsilateral to the hypertropic eye. Infants with congenital superior oblique palsies present with a head tilt, whereas older children and adults with decompensated congenital palsies complain of vertical and/or torsional diplopia.323 To diagnose a congenital superior oblique palsy, old photographs are helpful, often revealing a long-standing head tilt. Also, vertical fusional amplitudes frequently exceed the normal range of 3 to 4 prism diopters. The presence of a suppression scotoma when assessing diplopia or the presence of fusion also aids in establishing the chronicity of the condition as suppression is usually a childhood adaptation mechanism. Moreover, the presence of facial asymmetry may be associated with a longstanding head tilt from early childhood.176,202,338,528 The presence of facial asymmetry may not be a speciﬁc sign for congenital superior oblique palsy, however, because patients with acquired

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superior oblique palsy and heterotopic rectus muscles exhibited similar features of facial asymmetry.502 The causal relationship of the head tilt due to an abnormal superior oblique is not established.373 Hemifacial changes are often associated with plagiocephaly as a craniofacial anomaly, and craniofacial anomalies are commonly associated with anomalous extraocular muscles.124 2. The examiner also checks for bilateral and asymmetrical superior oblique palsies, because the larger paresis may “mask” the smaller until unilateral surgery is performed.274,280 Bilateral involvement should particularly be suspected after closed head injury. Findings that suggest bilaterality include alternation of hypertropia with ﬁxation, gaze, or head tilt; excyclotorsion of 10° or more; and V-pattern esotropia.286 3. Excyclodeviations usually occur with trochlear palsies, may accompany restrictions and myasthenia gravis, and are less commonly seen with skew deviations.494 The triad of skew deviation, head tilt, and incyclotorsion of the hypertropic eye is termed the ocular tilt reaction, an entity that can mimic fourth nerve palsy on the traditional three-step test.128 Therefore, examination for torsion, by double-maddox rod or simple fundoscopy, is essential in distinguishing a fourth nerve palsy from ocular tilt reaction.

INHERITANCE Rarely, congenital superior oblique palsy may be familial.28,198 The mode of inheritance in the described families has not been determined.

NATURAL HISTORY Long-standing congenital superior oblique palsy may decompensate in adulthood for a variety of reasons, including trauma, with the presenting symptom of vertical diplopia. As for traumatic cases, most cases of unilateral injury do resolve (see following). Also, after long-standing fourth nerve palsy, a “spread of concomitance” may be observed where the deviation in rightgaze and leftgaze are nearly equal, although the differential deviation in right versus left head tilt persists. This spread of concomitance has been attributed to a “contraction” of the ipsilateral superior rectus muscle.26

TREATMENT Most surgeons wait 6 to 12 months before deciding on strabismus surgery for traumatic cases, to await spontaneous resolu-

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tion of the deviation or stability in measurements. For congenital cases presenting with head tilt in infancy, surgery may be performed as soon as possible to correct the head posture and thus to aid in normal development of the neck muscles and the alignment of cervical vertebrae. It is unknown, however, whether early strabismus surgery can prevent or reverse facial asymmetry. For the large head tilts in infancy, a superior oblique tuck may treat the head tilt quickly; the beneﬁt of normalizing head posture with this procedure may outweigh the resultant iatrogenic Brown’s syndrome. For long-standing fourth nerve or superior oblique palsy, a variety of options exist. One approach is to operate on one muscle for vertical deviations of up to 15 prism diopters and to consider two-muscle surgery in deviations above 15 prism diopters. The ﬁrst choice of procedure is often ipsilateral inferior oblique muscle weakening. The second procedure often performed when the deviation is greater than 15 prism diopters is either ipsilateral superior rectus recession,26 when the vertical deviation is worse in upgaze, or contralateral inferior rectus recession, when the deviation is worse in downgaze.202 A fast and easy approach to deciding which muscle to weaken ﬁrst is to perform a “modiﬁed Parks three-step test”205 to determine which muscle is overacting and then to weaken that muscle ﬁrst. This modiﬁed three-step test is performed in the same manner as the traditional one, except for the ﬁrst step, in which the overacting vertical muscles are circled in each eye (instead of the traditional method of circling the presumed weak vertical muscles). In the case of bilateral palsy, bilateral inferior rectus recession and Harada–Ito procedures are recommended, both able to treat excyclotorsional diplopia.

PROGNOSIS When a child presents with a postinfectious, isolated trochlear palsy that cannot be explained as congenital, traumatic, restrictive, myasthenic, or neoplastic, the prognosis is good and observation alone is sufﬁcient. Overall prognosis for recovery of isolated fourth nerve palsies in adults and children was reported to be 53.5% combined (1000 total patients from 2 months to 91 years of age, 90% of whom were over 19 years and 75% of whom were over 35 years of age).424 Unilateral traumatic fourth nerve palsies in a series of 24 pediatric and adult patients (ages 7–78 years; mean, 35.4 years),

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46% of whom sustained minor head trauma, resulted in 75% resolution.483 Another series reported 65% resolution in unilateral but 25% in bilateral cases of traumatic fourth nerve palsy.479

THIRD NERVE PALSY ETIOLOGY

AND

SYSTEMIC ASSOCIATIONS

In childhood, a third nerve palsy typically keeps company with other neurological ﬁndings, which aid in localization and diagnosis (Table 12-6), but isolated palsies do occur and are generally congenital, traumatic, infectious, or migrainous.191,225,257,326,339,440 An acquired, isolated oculomotor nerve palsy in a child may also result from tumor, preceding viral illness, bacterial meningitis (most commonly pneumococcal, Haemophilus inﬂuenzae type b, or Neisseria meningitidis), or immunization.76,77,86,191,225,257,309, 326,339,347,430,440,446 Rarely, children may demonstrate gradually progressive paresis because of a slowly growing tumor1 or a truly cryptogenic oculomotor palsy. Posterior communicating aneurysms, although extremely rare in children, should be considered as well.313 Microvascular infarction due to atherosclero-

TABLE 12-6. Etiology of Infranuclear Third Nerve Palsy. Location/signs

Etiologies

Fascicle Ipsilateral cerebellar ataxia; contralateral rubral tremor; contralateral hemiparesis; vertical gaze palsy

Demyelination; hemorrhage; infarction (rare in childhood)

Subarachnoid space Papilledema; other cranial nerve palsies

Meningitis; trauma or surgery; tumor; increased intracranial pressure; uncal herniation

Cavernous sinus/superior orbital ﬁssure Ipsilateral Horner’s syndrome; ipsilateral IVth, Vth, VIth nerve involvement; proptosis; disc edema; orbital pain; conjunctival/episcleral injection

Cavernous sinus thrombosis; tumor; internal carotid artery aneurysm; carotid–cavernous ﬁstula; Tolosa– Hunt syndrome; pituitary apoplexy; sphenoid sinusitis, mucocele; mucormycosis

Orbit Ipsilateral IVth, Vth, VIth nerve involvement; proptosis; enophthalmos; disc edema; orbital pain; conjunctival/episcleral injection

Trauma; tumor; inﬂammation

Uncertain location

After febrile illness or immunization; migraine; idiopathic

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sis, hypertension, or diabetes mellitus, a common cause of isolated third nerve palsy in adults, is extremely rare in children.

CLINICAL–ANATOMIC CORRELATION The anatomic organization of the third nerve nucleus, like that of the sixth nerve nucleus, provides constraints that help differentiate the rare nuclear third nerve palsy from an infranuclear third nerve palsy. Because the superior rectus subnucleus supplies the contralateral superior rectus muscle, and the central caudal nucleus innervates both levator muscles, damage to a single oculomotor nerve nucleus gives rise to contralateral superior rectus weakness and bilateral ptosis. Also, because of the arrangement of the three medial rectus subnuclei and the visceral nuclei within the oculomotor nucleus, a nuclear third nerve palsy is not likely to produce isolated medial rectus involvement or unilateral pupillary involvement. In addition, other midbrain signs such as vertical gaze abnormalities are often associated with lesions of the oculomotor nucleus (see Fig. 12-6). Because the oculomotor nerve innervates the levator palpebrae superioris, the sphincter of the pupil and ciliary body, as well as four extraocular muscles (the medial rectus, superior rectus, inferior rectus, and inferior oblique), it is easy to identify a complete infranuclear third nerve palsy by the presence of ptosis; a ﬁxed, dilated pupil; and a “down-and-out” eye position resulting from the unopposed lateral rectus and superior oblique muscles (Fig. 12-10). However, third nerve palsies can be “partial”; any individual sign or combination of signs may be present and, if present, may be complete or incomplete. Numerous patterns can therefore arise.

CLINICAL FEATURES HISTORY

AND

ASSESSMENT/NATURAL

Oculomotor nerve palsies, like abducens and trochlear nerve palsies, should be distinguished from myasthenia and mechanical restrictions. Clinically observable involvement of the pupil or signs of oculomotor synkinesis (aberrant regeneration) establish involvement of the third nerve, assuming pharmacological and traumatic mydriasis can be excluded. The manner through which neural impulses become misdirected is not always clear.455 Misrouting of regenerating motor axons is ﬁrmly documented152,392,456 and corroborates the frequent clinical observation of the appearance of synkinesis at about 8 to

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B

C FIGURE 12-10. Patient with traumatic left third nerve palsy. The top photograph shows the classic appearance of a left third nerve palsy with ptosis and the eye in a down and out position. The left photograph shows full abduction, left eye. The bottom right photograph shows left eye with limited adduction. Note, there is lid retraction and miosis, left eye, on attempted adduction indicating aberrant innervation of the levator muscle and pupillary sphincter with part of the medial rectus nerve.

12 weeks after an acute palsy.277 However, aberrant regeneration cannot comfortably account for transient oculomotor synkinesis239,289,454 or spontaneous “primary” oculomotor synkinesis.66,105,289,436,493 Ephaptic transmission, conduction of a nerve impulse across a point of lateral contact, and synaptic reorganization of the oculomotor nucleus are two proposed theories of synkinesis.289,455 The presence of oculomotor synkinesis has not been reported with demyelination, but it does not otherwise narrow the differential diagnosis of third nerve palsy in the pediatric age group. Congenital third nerve palsy is usually incomplete and unilateral and is frequently associated with oculomotor synkinesis and “miosis” of the pupil in the affected eye.191,326,504 Although many children with congenital oculomotor nerve palsies have no associated neurological ﬁndings, some do,41 and a thorough neurological evaluation of these infants is suggested. If there are additional neurological signs or bilateral third nerve palsies, MRI may also provide useful information.175

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Rarely, paresis and spasm of the extraocular and intraocular muscles innervated by the third nerve may alternate, typically every few minutes, to produce oculomotor palsy with cyclic spasms.295 With few exceptions, these cycles accompany congenital, rather than acquired, oculomotor palsies and continue throughout life. In some instances, several months to several years may elapse between the discovery of the paresis and the onset of the cyclic spasms. Investigation is not necessary unless the third nerve palsy is acquired or there is progressive neurological dysfunction. The pathogenesis of this phenomenon remains obscure.272 Ophthalmoplegic migraine generally begins in childhood40 but may even be seen in infancy.13,534 It is an uncommon disorder despite the fact that 2.5% of children experience a migraine attack by age 7 and 5% by age 15.43 Symptoms of migraine in children include nausea, vomiting, abdominal pain, and relief after sleep in 90%.419 The headaches, which may be accompanied by an aura, are often unilateral and throbbing in quality. Family history is positive in 70% to 90%. With ophthalmoplegic migraine, the patient characteristically experiences pain in and about the involved eye, nausea, and vomiting; often the third nerve palsy ensues as the pain resolves. Full recovery of third nerve function within 1 to 2 months is typical, but resolution may be incomplete and oculomotor sykinesis has been reported.355 Multiple attacks may occur, and years may pass between episodes.133 Most patients with ophthalmoplegic migraine have normal angiograms, but one 31-year-old with recurrent episodes of ophthalmoplegic migraine, which had begun at age 5, and partial third nerve palsy since age 7, demonstrated a small perimensencephalic vascular anomaly.224 Aneurysms have been reported to cause isolated third nerve palsies during the ﬁrst and the second decades of life71,135,157,158,313,383 and carry a high risk of mortality or signiﬁcant morbidity if left undetected and untreated. On the other hand, aneurysms appear to be rare in children.158,495 Angiography with general anesthesia can be risky in the childhood age group, and the gap between the sensitivity of angiography and MRI for detecting aneurysms continues to narrow. The clinician assesses all these variables along with the history and physical examination to decide on the appropriate workup for each patient. For example, in the child under age 10 with a family history of migraine who presents with nausea, vomiting, and headache, followed by third nerve palsy as these symptoms resolve, that

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is, with typical ophthalmoplegic migraine, angiography may not be necessary.166 However, when a third nerve palsy acquired in childhood cannot be explained on the basis of the clinical examination or noninvasive neuroimaging, the cerebrospinal ﬂuid should be evaluated and angiography considered.

TREATMENT After diagnosis and treatment of the underlying disorder, observation of any recovery of oculomotor nerve function is necessary before surgical intervention. When partial or full recovery occurs, it often does so within 3 to 6 months but it may take 1 year or more. Surgical treatment includes strabismus surgery and ptosis correction. The latter is approached with caution in an eye that lacks a functional Bell’s phenomenon because of the risk of exposure keratopathy.

PROGNOSIS Two recent series have found fair to poor visual and sensorimotor outcome in oculomotor nerve palsy/paralysis of children with comparable mix of congenital, traumatic, and neoplastic cases.339,440 The best ophthalmologic outcome with measurable stereopsis was in the resolved cases (3 of 20; 15%) in the ﬁrst study, and in 4 of 31 patients with partial third nerve palsy in the second study, 2 of whom had spontaneous resolution. In the ﬁrst series, amblyopia therapy was most effective with congenital causes, but treatment results were poor with other causes; young children with posttraumatic and postneoplastic oculomotor nerve injuries demonstrated the worst ophthalmologic outcomes.

COMBINED OCULAR MOTOR NERVE PALSIES As the oculomotor, trochlear, and abducens nerves are in relatively close physical proximity from brainstem to orbit, it is not surprising that many diseases occurring at numerous locations can affect these nerves simultaneously.

CLINICAL ASSESSMENT The evaluation begins by establishing that the eye movement abnormality is due to cranial nerve disease rather than supranuclear lesions, disorders of the neuromuscular junction, restrictive or inﬂammatory myopathies, or chronic progressive “neuromyopathies,” for example, Kearns–Sayre syndrome. In the presence of a third nerve palsy, the fourth nerve function is

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tested by observing for intorsion of the affected eye in downgaze. If multiple ocular motor nerve palsies are indeed present, a thorough history and examination; neuroimaging of the rostral brainstem, cavernous sinuses, and orbits; and examination of the cerebrospinal ﬂuid (CSF) are typically necessary to distinguish between the myriad possible localizations and etiologies. Prompt diagnosis is particularly important for children with infections or pituitary apoplexy; the latter is often accompanied by severe headache, ophthalmoplegia caused by rapid expansion into the cavernous sinus, and rapid mental status deterioration.

ETIOLOGIES Processes in the brainstem (tumor, encephalitis), subarachnoid space (meningitis, trauma, tumor), and of uncertain localization (postinfectious polyneuropathy) tend to produce bilateral combined ocular motor nerve palsies whereas processes in the cavernous sinus/superior orbital ﬁssure (tumor, pituitary apoplexy, cavernous sinus thrombosis, carotid-cavernous ﬁstula) and orbit (trauma, tumor, mucormycosis) usually cause unilateral combined ocular motor nerve palsies. The ophthalmologist needs to be familiar with certain generalized neuropathies that may initially present with acute ophthalmoplegia. In a series of 60 patients with acute bilateral ophthalmoplegia, Guillain–Barre and Miller Fisher syndromes accounted for the diagnosis in 15 of 28 patients under age 45.253 The bulbar variant of Guillain–Barre syndrome (acute postinfectious polyneuritis) frequently presents as a rapidly progressive, painless ophthalmoplegia. Early in the course, involvement of eye movements may be incomplete and mimic either unilateral or bilateral oculomotor nerve palsies, but complete ophthalmoplegia with or without involvement of the pupils and accommodation typically evolves within several days. Partial ptosis usually accompanies severe limitation of eye movements,413 but levator function may be entirely normal or completely absent. Some degree of cranial nerve involvement occurs in about 50% of children with Guillain–Barre syndrome,413 and in the setting of rapidly progressing bilateral ophthalmoplegia, dysfunction of other cranial nerves, particularly bilateral facial nerve involvement, strongly supports the diagnosis of acute postinfectious polyneuritis. A variety of infections have been reported to precede Guillain–Barre syndrome in 50% to 70% of children; these include gastroenteritis, tonsillitis, measles, mumps, varicella, pertussis,

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hepatitis, Epstein–Barr virus, Campylobacter jejuni, coxsackie virus, and nonspeciﬁc upper respiratory infections. Two of these, varicella103,521 and acute Epstein–Barr virus infection,184 precede or accompany the onset of Guillain–Barre syndrome with noteworthy frequency in children and young adults. Paresthesias, often painful, commonly appear early in the course, and signs of meningeal irritation may also appear early in children. Although a rise in CSF protein levels without pleocytosis is the rule, it generally does not occur for several days to weeks after the onset of symptoms and, in a small percentage of patients, is not observed at all. The patient should be referred to a neurologist for management in a hospital setting with materials for tracheostomy and mechanical ventilation readily available. Ophthalmoplegia (external and sometimes internal), ataxia, and areﬂexia constitute Miller Fisher syndrome,155 and diplopia is usually the ﬁrst symptom. At least 20 children (under age 18 years) with Miller Fisher syndrome have been reported.50 A preceding febrile or “viral” illness may be reported with many of the same infectious agents previously listed. Although the eye movements often suggest unilateral or asymmetrical bilateral abducens pareses, many patterns have been reported including horizontal gaze palsy, upgaze palsy,249 pupil-sparing oculomotor nerve palsy, and pseudointernuclear ophthalmoplegia.30,125,478,520 All these eye movement patterns generally progress to severe bilateral ophthalmoplegia within 2 or 3 days. Ptosis and pupillary involvement may occur but are often absent.78 Limb and gait ataxia typically appear 3 or 4 days after the ophthalmoparesis but are, at times, concurrent with it. Areﬂexia is almost invariably present by the end of a week.141 An association with demyelinating optic neuropathy has also been reported.368,488 Miller Fisher syndrome is considered to be a variant of Guillain–Barre syndrome. However, there is some controversy as to the site of the lesion in Miller Fisher syndrome,8,315,414,415,488 whereas Guillain–Barre is clearly a peripheral neuropathy. Clinical observations suggesting the possibility of CNS involvement in Miller Fisher syndrome have included apparently supranuclear eye movement abnormalities314,459 and clouding of consciousness.8,50 In some cases, evoked potentials232 and MRI416 have been normal; in others, CT images121,541 and MRI136,163 have displayed clear abnormalities in the brainstem as well as in the cerebral white matter and cerebellum. In yet another group, absent F waves and H reﬂexes on peripheral nerve testing and

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markedly abnormal electroencephalograms suggested both peripheral and central involvement.50 Two neuropathological studies demonstrated normal CNS in both,119,378 and another showed inﬂammatory inﬁltration of peripheral and cranial nerve roots25; however, central chromatolysis in the nuclei of the third, fourth, ﬁfth, and twelfth nerves and of the anterior horn cells has also been reported.186 Additionally, anticerebellar antibody has been found to be reactive to a signiﬁcantly greater number of bands on Western blotting of serum from Miller Fisher patients (6 of 7) compared to that of Guillain–Barre (3 of 6) or healthy controls (4 of 10).227 As with acute postinfectious polyneuritis, if the CSF is examined late enough in the course, the protein concentration is elevated in most cases.141 A useful diagnostic tool is the presence of antiganglioside antibodies in serum of patients with Guillain–Barre and Miller Fisher syndromes. Patients with Guillain–Barre syndrome subsequent to Campylobacter jejuni enteritis frequently have IgG antibody to GM1 ganglioside. Miller Fisher syndrome is associated with IgG antibody to GQ1b and GT1a ganglioside in 90% of cases.527,539 Moreover, acute ophthalmoparesis without ataxia has also been found to be associated with anti-GQ1b antibody, suggesting that this is a milder variant of Miller Fisher syndrome.539 These antibody ﬁndings are evidence for the molecular mimicry theory of postinfectious autoimmune pathology. Despite its dramatic and alarming presentation, Miller Fisher syndrome generally has a benign prognosis. Careful observation is, however, recommended because ophthalmoplegia occurred early in one case of childhood Guillain–Barre syndrome that progressed to respiratory failure.179 Occasionally, “relapsing Miller Fisher syndrome” appears to occur,434,506 which should not be confused with recurrent ocular motor palsies that may accompany a rare familial syndrome of recurrent Bell’s palsy.9 Treatment of Guillain–Barre and Miller Fisher syndromes may, in severe cases, require plasmapheresis or intravenously administered immunoglobulin.241,538 Acute hemorrhagic conjunctivitis caused by enterovirus 70 can be accompanied by dysfunction of any of the cranial or spinal motor nerves,220,246,513 resulting in a polio-like paralysis (radiculomyelitis) in approximately 1 in 10,000 patients infected with this virus.535 Cranial nerve involvement occurred in 50% of the patients in one series.246 Solitary seventh or ﬁfth nerve palsies were most common, followed in frequency by combined ﬁfth and

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seventh nerve palsies. Prognosis correlates with severity and pattern of cranial nerve involvement; patients with mild weakness and involvement of cranial nerves VII, IX, and X tend to resolve fully, whereas those with severe weakness and involvement of cranial nerves III, IV, V, and VI often do not signiﬁcantly improve. Optic atrophy may also occur. Treatment is only symptomatic.

Anomalies of Innervation Some ocular motility disturbances, both congenital and acquired, arise when an inappropriate nerve or nerve branch innervates an extraocular muscle. Such “miswiring” immediately suspends the laws of extraocular motor physiology (e.g., Hering’s and Sherrington’s laws) and produces bizarre, intriguing eye movements. In certain cases, electromyographic (EMG) and pathological studies have conﬁrmed the defective anatomy and physiology underlying the clinical presentation. Although miswiring can generate many types of abnormal eye movements, only the more common anomalous motility patterns are detailed here.

SIXTH NERVE DUANE’S SYNDROME Duane’s syndrome is characterized by retraction of the globe and narrowing of the lid ﬁssure on attempted adduction as well as limited eye movements. Three forms of abnormal motility have been classiﬁed217: Type I: limited abduction with intact adduction (Fig. 12-11) Type II: limited adduction with intact abduction Type III: limited abduction and limited adduction Incidence Duane’s syndrome has been reported to account for 1% to 4% of all strabismus cases.122 Etiology Electromyographic data indicate that the medial and lateral recti contract simultaneously, that is, they “cocontract,” and may thereby produce both the retraction of the globe into the orbit and the limitation of eye movement.216,217,308 One can speculate as to how different distributions of inappropriate neural input from the oculomotor and abducens nerves to the lateral and medial recti could produce each of the three patterns of limited ocular motility seen in Duane’s syndrome. This

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FIGURE 12-11. Duane’s syndrome, left eye. This montage demonstrates the limitation of abduction (middle, right photo), palpebral lid ﬁssure narrowing on adduction (middle, left photo), upshoot in adduction (top, left photo), and “Y” pattern (middle, top photo) seen with Duane’s syndrome.

aberrant innervation is thought to be a result of congenitally deﬁcient innervation of the VIth nucleus, leading to a ﬁbrotic lateral rectus muscle (Fig. 12-12). Neuropathological investigations of three patients with Duane’s syndrome have all revealed aplasia or hypoplasia of the abducens nucleus and nerve, and in two of these cases, branches of the third nerve “substituted” for the defective sixth nerve by supplying some of its ﬁbers to the lateral rectus. The ﬁrst case was unilateral and demonstrated a hypoplastic lateral rectus muscle in addition to hypoplasia of the abducens nucleus and nerve.310 In a second patient with bilateral type III Duane’s syndrome, both abducens nuclei and nerves were absent; also, both lateral recti were found to be partially innervated by the inferior division of the oculomotor nerves and were histologically normal in innervated areas but ﬁbrotic in areas not innervated.213 The third patient had unilateral, left type I Duane’s syndrome and showed, as did the previous case, absence of the sixth nerve, partial innervation of the lateral rectus by the inferior division of the oculomotor nerve, and ﬁbrosis of the lateral rectus muscle in areas not innervated. However, although the left abducens nucleus was hypoplastic, containing less than half the number of neurons seen in the right nucleus, both medial longitudinal fasciculi were normal and the remaining cell bodies in the nucleus were interpreted to be internuclear neurons. This

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ﬁnding corroborates the clinical observation that, in unilateral type I Duane’s syndrome, adducting saccades in the unaffected eye are usually normal.177,322,333 This ﬁnding also indicates an exquisitely speciﬁc neural deﬁcit. Electrophysiological techniques such as auditory evoked potentials237 and eye movement recordings351,537 have suggested that there may be other associated brainstem dysfunction, but these studies have not produced conclusive evidence or have not been reproducible.403,481 “Upshoots” and/or “downshoots” on attempted adduction are common motility ﬁndings. Theoretically, the cause of the upshoots and downshoots may be mechanical, innervational, or a combination of the two. In most cases, the mechanics of the lateral rectus seem to be largely responsible because weakening or eradicating the action of a tight lateral rectus results in signiﬁcant reduction or elimination of upshoots and downshoots. The “bridle-effect theory” postulates that vertical sideslip of a tight lateral rectus across the adducting globe produces these movements234,510; however, neuroimaging has not conﬁrmed vertical displacement of the lateral rectus during upshoots and downshoots.62,511 In certain individuals, an innervational anomaly may account for upshoots and downshoots. For example, one of the authors (B.N.B.) has observed that continued severe upshoot on adduction in a patient whose lateral rectus was detached from the globe and allowed to retract far

FIGURE 12-12. Proposed embryonal etiopathogenesis of Duane’s syndrome as a congenitally deﬁcient innervation syndrome. The developing cranial nerves have a “trophic” function on the developing mesenchyme of the future extraocular muscles. If there is late or no innervation to the developing mesenchyme, the muscle becomes dysplastic, ﬁbrotic, and inelastic. If there is early aberrant innervation of the developing mesenchyme by cranial nerve III, the lateral rectus has a “normal” architecture but abnormal innervation, leading to limited abduction only (type I). The later during embryogenesis the innervation, the more dysplastic the lateral rectus, leading to limited adduction as well (type III). The balance between the quantitative amount of aberrant innervation and the degree of lateral rectus ﬁbrosis creates relatively different patterns of abduction and adduction, leading to the different “types” of Duane’s syndrome. Type II Duane’s syndrome (not depicted) may be caused by more innervation from the third cranial nerve to the lateral rectus compared to the medial rectus. Dotted lines represent absent or hypoplastic innervation; dashed lines represent later onset of innervation; thickness of lines represents quantitative amounts of innervation. LR, lateral rectus; MR, medial rectus; III, oculomotor nucleus; VI, abducens nucleus.

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into the orbit before suture adjustment. In addition, there is EMG evidence for cocontraction of appropriate cyclovertical muscles and the lateral rectus during upshoots and downshoots217,322,443; such cocontraction could play a substantial role in some cases. Clinical Features and Natural History Most large series indicate that females represent about two-thirds of cases and that the left eye is affected in about two-thirds of unilateral cases. Approximately 75% are type I; type III accounts for most of the rest, and type II is quite rare. Types I and II may occasionally coexist in the 10% to 20% of cases that are bilateral. Many Duane’s syndrome patients are orthotropic in primary position or with a small head turn and have excellent binocular function.229,391,402 Although amblyopia can occur in the involved eye, the reported incidence of amblyopia as well as anisometropia varies widely.448,491 Most Duane’s syndrome patients ignore or are unaware of sensory disturbances,300 but occasionally an older child presents with “acute” awareness of diplopia in the appropriate ﬁelds of gaze. As mentioned, upshoots and downshoots on attempted adduction may occur and may be accompanied by A, V, or X patterns, giving the appearance of oblique muscle dysfunction. Clinical Assessment Other diseases should be considered in the differential diagnosis. Rarely, acquired orbital disease may produce limitations of abduction and retraction, thereby mimicking Duane’s syndrome. This effect has been observed with medial orbital wall fractures, ﬁxation of muscle by orbital metastases, orbital myositis, and a variety of other conditions.165,266,367,469 Systemic Associations Although Duane’s syndrome is usually an isolated ﬁnding, it may accompany any of a multitude of other congenital anomalies in 5% to 57% of cases (Table 12-7).307,363,377 Inheritance Familial cases are not uncommon, and an autosomal dominant mode of inheritance best ﬁts most, but not all, of the reported pedigrees.126 Duane’s syndrome, sensorineural deafness, upper limb defects, facio-auriculo-vertebral anomalies, and genitourinary and cardiac malformations appear as isolated ﬁndings or in combination throughout certain families and may all, perhaps, be ascribed to a highly pleiotropic autosomal dominant gene that is frequently nonpenetrant.198a,361 Studies of

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TABLE 12-7. Congenital Anomalies Associated with Duane’s Syndrome. Structure

Associated anomalies

Ocular/external

Microphthalmos; coloboma; heterochromia iridis; ﬂocculi iridis; congenital cataract33,34,363 Ptosis; nevus of Ota; hypertelorism; prominent epicanthus33,34,210,377,448 Epibulbar dermoid307,363,377,379

Neural

Optic nerve anomalies34,120,248,261,307,377; DeMorsier syndrome5 Sensorineural deafness261–264,307,448 Seventh nerve palsy106,307,377,428 Marcus Gunn jaw winking230,307 Gusto-lacrimal reﬂex58,307,393 Fourth nerve palsy307 Möbius syndrome307

Musculoskeletal

Craniofacial anomalies; skeletal anomalies; Klippel–Feil syndrome; Goldenhar’s syndrome; Marfanoid hypermotility syndrome; cleft lip/palate; muscular dystrophy34,35,106,212,261–264,307,361,363,377,379,393,421,448

Miscellaneous

Cardiac anomalies35,307,377 Genitourinary anomalies106,377 Noonan syndrome Fetal alcohol syndrome211 Congenital panhypopituitarism107 Oculocutaneous albinism208

monozygotic twins have revealed both concordance and discordance in more than one family.207,247 Two recent reports of large families with autosomal dominant Duane’s syndrome, one in the U.K. and the other in Mexico, have both found linkage to chromosome 2q31.20,148 Other reports have found deletions in chromosome 8q in patients with Duane’s syndrome associated with other abnormalities such as mental retardation and hydrocephalus.79,505 Treatment A patient with unacceptable primary position deviation, head position, globe retraction, upshoot, or downshoot may require surgery. All these factors as well as the relative contributions of mechanical and innervational factors are considered during surgical planning. As a general recommendation, resections of the horizontal recti of an affected eye is usually avoided because this may increase globe retraction. Otherwise, the surgical approach is individualized.275 Depending on the situation, a wide variety of techniques may prove helpful, including transposition of the vertical recti with or

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without medial rectus recession,169,331 Y-splitting of the lateral rectus,410 adjustable sutures,388 and posterior fixation sutures.293,510 Prognosis Recession of horizontal rectus muscle eliminates the face turn in 79% of cases and signiﬁcantly reduces the face turn in most of the remaining patients.276,388 Undercorrection of primary position esotropia may occur postoperatively as the amount of recession needs to be larger than indicated in the traditional tables for concomitant strabismus; rerecession is recommended for these cases if the initial recession was less than 8 mm or if forced duction testing still indicates restriction. The occasional overcorrections may be reversed by advancing the recessed muscle or recessing the antagonist horizontal rectus muscle if tight.171,348,353

SYNERGISTIC DIVERGENCE Synergistic divergence is a striking motility pattern consisting of an adduction deﬁcit with simultaneous bilateral abduction on attempted gaze into the ﬁeld of action of the involved medial rectus.109,514,525 As with Duane’s syndrome, cocontraction of the lateral and medial recti has been demonstrated on EMG,525 and it has therefore been suggested that synergistic divergence may be placed along the Duane’s “spectrum” of congenital anomalous innervation. In this conceptual scheme, synergistic divergence is similar to type II Duane’s syndrome, except that the larger part of the branch of the third nerve “intended” for the medial rectus is misdirected to the lateral rectus. The globe retraction characteristic of Duane’s syndrome does not accompany synergistic divergence, presumably because there is so little innervation to the medial rectus. However, this hypothesis has not been veriﬁed by clinicopathological study, and saccadic velocity studies in two patients indicate that the abducens nerve may not necessarily be absent or severely hypoplastic.188 Synergistic divergence has been observed as early as 5 months of age,108 may be bilateral,187,188,486 and has been associated with other abnormalities including Marcus Gunn jawwinking,72,73,187 ipsilateral congenital Horner’s syndrome,238 arthrogryposis multiplex congenita,109 congenital ﬁbrosis syndrome, and oculocutaneous albinism.72,73 Surgical crippling of the ipsilateral lateral rectus has been combined with a variety of other procedures such as medial rectus resection and superior oblique tenotomy and inferior

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330

oblique myectomy to eliminate the simultaneous abduction as well as to correct the exotropia in primary position.188 Other types of anomalous innervation that may involve the sixth nerve include congenital or acquired synkinesis of the levator and lateral rectus during abduction,242,343 acquired trigemino-abducens synkinesis with abduction accompanying jaw movements,312,349,453 congenital twitch abduction on attempted upgaze,271 or lateral gaze synkinesis on downward saccades.503

THIRD NERVE OCULOMOTOR SYNKINESIS Oculomotor synkinesis (aberrant regeneration of the third nerve) commonly accompanies third nerve palsies, usually those of congenital or traumatic origin, but also those caused by aneurysm, migraine, or tumor. This condition is discussed in detail in the section on third nerve palsies. Although oculomotor synkinesis is, perhaps, the most familiar form of anomalous innervation involving the oculomotor nerve, other patterns do occur.

VERTICAL RETRACTION SYNDROME Vertical retraction syndrome is exceedingly rare with only several case reports in the literature.258,376,389,433,518 Typically, elevation or depression of the globe is limited, and when attempted, it is associated with narrowing of the lid ﬁssure and retraction. There may be an associated horizontal deviation that is greater with gaze in the direction of the limited vertical eye movements. Forced ductions are positive, although this does not preclude a central mechanism. EMG study of one patient revealed lateral rectus muscle contraction on upgaze and downgaze. Eye movement recordings of this and two other patients in the same study showed a twitch abduction of the occluded eye on upward saccades, followed by a postsaccadic drift back and a slower abduction in downgaze; this phenomenon was seen in each nonﬁxing of all three patients, suggesting a synergistic innervation between the abducens nerve and the upper and lower divisions of the oculomotor nerve. EMG in one atypical case of vertical retraction syndrome showed cocontraction of the vertical recti in upgaze, downgaze, and adduction, and electro-oculography was also consistent with

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an anomalous innervational pattern.389 The clinical ﬁndings included exotropia; poor elevation and adduction; retraction of the globe on upgaze, downgaze, and adduction; and downshoot on adduction.

MARCUS GUNN JAW-WINKING Marcus Gunn jaw-winking is not usually accompanied by abnormal eye movements but is included here as another instance of anomalous innervation. This congenital trigemino-oculomotor synkinesis links innervation of jaw and eyelid levator muscles and is characterized by congenital ptosis, usually unilateral, with elevation of the ptotic lid when the jaw is moved. This ipsilateral associated ptosis accounts for 5% to 10% of all congenital ptosis.57,193 Etiology Because normal subjects demonstrate EMG cocontraction of the muscles supplied by the oculomotor nerve and certain muscles of mastication supplied by the trigeminal nerve,427 Marcus Gunn jaw-winking may represent an exaggeration of a physiological synkinesis that is normally present but clinically undetectable. The precise mechanism for failure of higher inhibition remains unclear. EMG evidence and histological study of the levator muscles suggest an underlying brainstem process because the levator muscles are involved bilaterally.204,299,427 Clinical Features There are two major categories of trigemino-oculomotor synkinesis. The ﬁrst, and most common, consists of external pterygoid-levator synkinesis and is characterized by lid elevation when the jaw is projected forward, thrust to the opposite side, or opened widely. In the second form, internal pterygoid-levator synkinesis, lid elevation is triggered by clenching of the teeth. Rarely, a number of stimuli other than pterygoid contraction can cause eyelid elevation, and these include smiling, inspiration, sternocleidomastoid contraction, tongue protrusion, and voluntary nystagmus. Conversely, in an unusual case of trigemino-oculomotor sykinesis, pterygoid contraction was associated with contraction of the inferior rectus rather than the levator, thereby producing monocular bobbing eye movements rather than eyelid elevation.356 Marcus Gunn jaw-winking typically presents shortly after birth with rhythmic elevation of the affected upper lid during feeding. The ipsilateral associated ptosis may be of any degree of severity. A significant number of patients have amblyopia,

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anisometropia, strabismus, superior rectus palsy, or double elevator palsy.57,193 Natural History It is interesting to note that, in many cases, parents remark that the synkinesis seems less apparent as the child becomes older. As this observation is not supported by objective examination, it may occur because the child learns to control both lid position and excursion. Systemic Associations Marcus Gunn jaw-winking can be bilateral; has been reported in association with other forms of anomalous innervation such as synergistic divergence, Duane’s syndrome, and trigemino-abducens synkinesis; and is rarely familial or associated with heritable diseases such as Waardenburg syndrome, Rubinstein–Taybi syndrome (author’s observation; M.M.), Hirschsprung megacolon, neuroblastoma, and neuroﬁbromatosis type 1.94,268,316 Treatment Strabismus, amblyopia, and anisometropia are treated when necessary. Surgical management of the ptosis may be achieved by conventional levator resection in mild cases of jaw-winking. In moderate to severe cases, bilateral levator excision and bilateral frontalis suspension have been shown to provide satisfactory correction of both jaw-winking and ptosis. The frontalis suspensions may be achieved by using fascia lata, either autologous or homologous, or strips of the levator muscle after transsecting the muscle, but still attached distally via the aponeurosis to the tarsus.45,259

SEVENTH NERVE The seventh nerve may also be involved in several anomalous innervational patterns that do not affect eye movements but may present to the ophthalmologist.

INTRAFACIAL SYNKINESIS Intrafacial synkinesis commonly appears after peripheral facial nerve palsies; branches of the regenerating seventh nerve are misrouted to inappropriate muscles. Frequently, for example, the orbicularis oculi contracts simultaneously with lower facial muscles, and there may be signiﬁcant narrowing of the palpebral ﬁssure with smiling. Other patterns can occur and, on occasion, are bothersome enough for a patient to require botulinus toxin injection or surgery.22,390,411

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MARIN–AMAT SYNDROME This syndrome, also known as inverse Marcus Gunn phenomenon, is a rare disorder in which the upper eyelid falls when the mouth opens. This syndrome is observed after peripheral facial nerve palsies and has been suggested to be a result of aberrant reinnervation. However, EMG shows inhibition, rather than excitation, of the affected levator muscle during external pterygoid contraction,296 and absence of orbicularis oculi activity may differentiate this condition from the typical forms of intrafacial synkinesis. Wide jaw opening causes synkinetic contraction of the orbicularis oculi and lid closure, possibly triggered by stretching of the facial muscles.394

DISORDERS AT THE NEUROMUSCULAR JUNCTION Myasthenia Gravis in Infancy Myasthenia gravis in the infant takes one of three clinical forms.

TRANSIENT NEONATAL MYASTHENIA Transient neonatal myasthenia is seen in approximately one of seven infants born to mothers with myasthenia gravis. All these babies develop a weak cry and difﬁculty sucking in the ﬁrst several days of life, and about half become generally hypotonic. This condition, caused by antiacetylcholine receptor antibody (anti-AChR antibody) received by the baby from the mother’s circulation,292 responds promptly to anticholinesterase agents but will resolve in 1 to 12 weeks if untreated.344,530 There is no relapse or long-term sequela.

FAMILIAL INFANTILE MYASTHENIA GRAVIS Familial infantile myasthenia is rare, appears in children of mothers without myasthenia gravis, and presents in early infancy with ptosis, poor suck and cry, and secondary respiratory infections. Episodic crises of severe respiratory depression and apnea are precipitated by fever, excitement, or vomiting.151,180,406 Other features include hypotonia, proximal muscle weakness, and easy fatigability, but the extraocular muscles are usually not involved. Inheritance of familial infantile myasthenia gravis has been reported to be autosomal recessive

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with localization to the telomeric region of chromosome 17, on 17p13.90 A candidate gene under study for this disease in the 17p region is synaptobrevin-2, a synaptic vesicle protein; this protein probably participates in neurotransmitter release at a step between docking and fusion.221 This disorder responds to anticholinesterase medications and tends to ameliorate with age.

CONGENITAL MYASTHENIC SYNDROMES A third type of myasthenia seen in infants is the group of congenital myasthenic syndromes, a heterogeneous group of disorders that may affect presynaptic or postsynaptic mechanisms. Various acetylcholine receptor subunit defects as well as genetic defects in endplate acetylcholinesterase have been related to different congenital myasthenic syndromes.144 The frequency of congenital myasthenic syndromes varies from 8% to 21% in reported series of childhood myasthenia gravis, reportedly higher where consanguineous marriages are frequent.18,340 In the fetal period, decreased fetal movements have been reported, resulting in arthrogryposis multiplex congenital, congenital ﬂexures, and contractures of multiple joints.498 Affected patients are born to mothers without myasthenia and may demonstrate ptosis and ophthalmoparesis during infancy. Severe generalized weakness may also present in the postnatal period with frequent apneic episodes, recurrent aspiration, failure to thrive, and poor sucking. Other patients may present during the ﬁrst or second year of life with ocular signs and only mild systemic signs. Although ptosis was reported to be present in all of seven patients in one series,340 it was generally mild and not incapacitating. These disorders persist throughout life and can be distinguished from acquired myasthenia gravis and from each other by combining clinical, electrophysiological, ultrastructural, and cytochemical investigations.144–146 Tensilon testing can be positive, and a patient may respond to a trial of pyridostigmine. Presence of anti-AChR antibody excludes this disease.340 Inheritance in one type termed slow-channel congenital myasthenia gravis has been attributed to mutations in the AChR subunit genes, and depending on which subunit is mutated, the disease is transmitted in an autosomal dominant or autosomal recessive fashion. Treatment in congenital myasthenic syndrome patients is generally supportive, and the use of acetylcholinesterase

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inhibitors is disease speciﬁc. Surgery for stable strabimsus in a child can yield a stable long-term result.340

Autoimmune Myasthenia Gravis INCIDENCE Acquired myasthenia gravis affects overall about 1 in 20,000 per year to 0.4 in 1,000,000 per year.519 Girls are affected two to six times as frequently as boys, and the incidence of the condition increases progressively through childhood until the end of the second decade of life. Afer the age of 50 years, males predominate; the mean age of onset in women is 28 years and in men 42 years.519 Among the various childhood forms of myasthenia gravis, a recent series identiﬁed 25 (71%) of 35 children as having the autoimmune disease.340

ETIOLOGY Acquired myasthenia gravis is an autoimmune disorder. The myasthenic patient has fewer available skeletal muscle acetylcholine receptors because of antibodies produced against these receptors130 and also because of complement activation.16 Neuromuscular transmission is thereby poised to fail. Normally, with repetitive stimulation of a motor nerve, the amount of acetylcholine released from that nerve diminishes. In the delicately balanced myasthenic, this decrease in neurotransmitter may well lead to a failure of muscular response. In this context, it is easy to understand why muscle fatigue is the clinical hallmark of myasthenia gravis and why the constant activity of the extraocular muscles, among other activities,243,354 particularly predisposes them to demonstrate fatigue. The exact reasons for predilection for the extraocular muscles are under study, one explanation potentially lying in the differential expression of acetylcholine receptor subunits in extraocular versus skeletal muscle.47,244,301 A number of medications are known to produce myasthenia gravis in normal individuals or to exacerbate already existing disease. The list includes D-penicillamine, antibiotics, anticonvulsants, intravenous contrast dye, anticholinesterase agents, neuromuscular blocking agents, antiarrhythmic drugs, phenothiazines, beta-blockers, and quinine. For example, myasthenia produced by D-penicillamine is indistinguishable from

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primary acquired myasthenia clinically, immunologically, and electrophysiologically.519

CLINICAL FEATURES Several general clinical observations may be made concerning myasthenia gravis. Muscle weakness is not accompanied by other neurological signs; muscle function, which may ﬂuctuate even within the course of an ofﬁce visit, is improved by cholinergic medications; and extraocular, facial, and oropharyngeal muscles are most commonly involved. Beyond this, there are numerous variations of presentation, and no single sign is solely reliable.

NATURAL HISTORY Of patients who present initially with purely ocular symptoms and signs, 50% to 80% subsequently develop generalized myasthenia within about 2 years.519 In a large study of 1487 patients with myasthenia, 53% presented with ocular symptoms.183,519 Of the entire group of myasthenic patients in this study, 15% continued to demonstrate purely ocular manifestations (with follow-up to 45 years; mean, 17 years). Of the 40% of patients in this study with strictly ocular involvement during the ﬁrst month after onset of symptoms, 66% developed generalized disease. Of these who subsequently developed generalized disease, 78% did so within 1 year, and 94% within 3 years after onset of symptoms and signs. In a series of 24 children in Toronto with acquired autoimmune myasthenia (age, 11 months to 16 years; median age, 4.7 years), 14 (58%) patients initially had ocular involvement only (median follow-up time, 2.6 years). Of these 14, 5 (36%) progressed to generalized myasthenia gravis in a mean time of 7.8 months (range, 1–23 months). Patients with ocular myasthenia presented at an average of 6.8 years; those with systemic disease presented on average at 7.1 years.340

CLINICAL ASSESSMENT Variable diplopia or ptosis most often prompt an ophthalmologic evaluation. Patients with these symptoms are evaluated for signs and symptoms of generalized myasthenia such as facial weakness, dysphonia, arm or leg weakness, chewing weakness, and respiratory difﬁculties. In “ocular myasthenia,” however,

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the ﬁndings are restricted to the levator and extraocular muscles. Because there is no stereotypical myasthenic eye movement, this diagnosis should be considered in any child with an unexplained, acquired ocular motility disturbance and clinically normal pupils, particularly when the deviation is variable, whether or not ptosis is present. Any pattern of abnormal motility is suspect, including an apparent gaze palsy, internuclear ophthalmoplegia,167 isolated cranial nerve palsy,423 one and onehalf syndrome,116,468 incomitant strabismus, accommodative and vergence insufﬁciency,101 and gaze-evoked nystagmus.250,288 Prolonged OKN may demonstrate slowing of the quick phases; large saccades may be hypometric; small saccades may be hypermetric; and characteristic “quiver movements,” which consist of an initial small saccadic movement followed by a rapid drift backward, may be seen.46,288 In addition to the eye movements, lid function is assessed. Ptosis can be elicited or accentuated by fatiguing the levator palpebrae superioris with prolonged upgaze or repeated lid closure. Because Hering’s law of equal innervation applies to the levator muscles as it does to the extraocular muscles, the contralateral lid may be retracted but falls to a normal position when the ptotic lid is lifted with a ﬁnger. Through the same mechanism, in bilateral ptosis, manual elevation of one lid increases the amount of ptosis on the other side by diminishing the amount of innervation necessary to ﬁxate. Cogan’s lid twitch sign can be elicited in some myasthenic patients by having the patient look down for 20 s and then making an upward saccade to the primary position; the lid twitches upward one or more times and then slowly drops to its ptotic position. Finally, the orbicularis oculi muscles are often weak, and the patient may not be able to sustain lid closure. Examination of the patient before and after the administration of anticholinesterase agents is, arguably, of more limited use in children than in adults. This method may be most helpful in children whose history and physical examination do not permit a clear diagnosis yet who have such signiﬁcant deﬁcits in lid elevation or ocular motility that a response is easily observed. A positive test consists of the direct observation of a weak muscle becoming stronger after the administration of intravenous edrophonium hydrochloride (Tensilon) or intramuscular neostigmine methylsulfate (Prostigmin). The initial dose is 2 mg, given up to 10 mg total. The onset of action for Tensilon is 30 s, lasting up to 5 min. This drug is contraindicated

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in patients who are elderly or have heart disease, and other workup should be performed before considering the Tensilon test. Intramuscular Prostigmin is longer acting than Tensilon and allows more time for measurement of changes, but its absorption rate and hence onset of action are quite variable; its onset of action is generally between 15 to 20 min and the peak response occurs about 30 to 40 min after administration. In children the dose is 0.02 mg/kg, always with a total of less than 1.5 mg; and in adults the dose is 1.5 mg, with atropine 0.6 mg, coadministered.279 Choice of drug can be individualized according to the endpoints that are being assessed and to the ability of the child to cooperate. To make a decisive observation, it is important, both before and after giving these drugs, to quantitate as accurately as possible the function of the affected muscle(s) through measurement of pertinent indicators such as lid height in primary position, levator function, saccadic velocities, ocular movement, ocular alignment, and orbicularis strength. After administering Tensilon, the examiner observes for tearing and lid fasciculations as evidence of cholinergic effect, and draws no conclusion if a paradoxic decrease in muscle function occurs, because this may happen in the presence or absence of myasthenia. Positive responses after either drug are fairly reliable evidence for myasthenia but can, on rare occasions, occur in nonmyasthenic patients. False-negative responses, however, are common and therefore do not exclude myasthenia gravis. Alternatively, a rest test may be used by allowing the patient to rest with eyes closed for a period of 10 to 15 min.337 An “ice test” has also been reported to improve ptosis173,278,425 and motility142 after applying an ice pack to the eyes for 2 to 5 min. However, subsequent report of four patients337 revealed no difference among an ice test, a heat test, or a rest test, so long as the rest period was at least 10 to 15 min. Further diagnostic testing may include anti-AChR antibody titer and electromyography. EMG is particularly useful in generalized myasthenia but is difﬁcult to perform in a frightened, uncooperative child. The electromyographer looks for a characteristic decrement in the muscle action potentials with repetitive supramaximal nerve stimulation and for the “jitter phenomenon” on single muscle ﬁber studies, difﬁcult responses to elicit and observe even in a cooperative patient. Anti-AChR antibody is most helpful in generalized myasthenia as it is reportedly present in 80% to 90% of those patients but only 50%

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or fewer of ocular myasthenics.149,463,519 According to other reports, speciﬁcally on juvenile myasthenia gravis patients, the frequency of postive AChR antibody was between 56% and 63%.4,15,19

SYSTEMIC ASSOCIATIONS Associated immune disorders to be considered in children include rheumatoid arthritis, juvenile-onset diabetes mellitus, asthma, and thyroid disease; neoplasia (breast cancer, uterine cancer, carcinoma of the colon, pinealoma) is also seen.408 Thymoma rarely occurs in children although it is recognized to accompany 10% of myasthenia gravis.

INHERITANCE Inheritance is usually sporadic. Approximately 1% to 4% of cases are familial without a clear Mendelian pattern. This familial predisposition may be due to predilection for autoimmunity in general.

TREATMENT Once the ophthalmologist diagnoses or strongly suspects myasthenia, a neurologist generally directs further testing and treatment. The ophthalmologist’s role remains important, however. In addition to monitoring the motility and lid dysfunction and providing symptomatic relief for these disorders, the ophthalmologist should be alert to the possibility of amblyopia. If not promptly detected and attended to, amblyopia can be extremely difﬁcult to treat, particularly when there is sufﬁcient ptosis to necessitate taping or a ptosis crutch for the lid during occlusion of the sound eye. Current therapy aims to increase the amount of acetylcholine available through the use of anticholinesterase agents or to diminish the autoimmune reaction with corticosteroids, other immunosuppressive agents, such as azathioprine, cyclosporin A, and mycophenolate mofetil,93,150 plasmapheresis, or thymectomy. Supervision of these treatments is clearly in the bailiwick of the neurologist. It is worth noting that anticholinesterase agents are not as effective in ameliorating ocular motility as they are for other manifestations of myasthenia149 nor are they as effective as steroids462 or other treatments directed against the autoimmune response.431 However, because

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of the risks and complications, the use of steroids, immunosuppressives, plasmapheresis, and thymectomy in pure ocular myasthenia gravis remains controversial.68,365,441 In a recent pilot study, cyclosporin A was found to be effective in a series of eight patients, resulting in complete remission in seven of the eight, with a mean follow-up of 14 months; the eighth patient was noncompliant.80 Strabismus surgery has been performed on patients with stable deviations of at least 5 months, using conventional strabismus surgical techniques.115,360 The presence of systemic disease is an important consideration in deciding on the method of anesthesia, although general anesthesia is not an absolute contraindication when the disease is clinically controlled.

PROGNOSIS The prognosis for survival, improvement, and remission in a child with myasthenia gravis is better than that in an adult, according to most studies.327,408,462 Rodriquez and coworkers408 studied 149 children who were less than 17 years old at the onset of autoimmune myasthenia gravis and had a median follow-up of 17 years with minimum follow-up of 4 years. An estimated 80% of these patients were alive at age 40, about 90% of the survival expected in the general population. Improvement or remission was seen in 79% of the 85 patients who underwent thymectomy and 62% of the remaining 64 patients. In the smaller Toronto series, children required an average of 2 years on medication before entering remission.340 Complete remission in adults has been reported as 40% to 70%, generally achieved after 1 to 3 years of treatment.519 In 9% of children in the Rodriquez series, the disease remained strictly ocular; this is comparable to the 14% found in a large adult series observed over a similar interval.183 In the Toronto series, 38% of the 24 children remained strictly ocular, although the mean follow-up period was 3.5 years.340 Children with ocular myasthenia gravis may also show prolonged remissions and respond well to steroid therapy on relapse.412,437 The result of strabismus surgery for myasthenia gravis has reportedly been favorable in two studies, after a follow-up of 4 months to 14 years (median, 12 months).115,360 In these two studies combined, 2 of 10 patients required reoperations, and 1 of the 10 required prisms postoperatively.

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Botulism Numerous pharmacological agents and toxins may interfere with transmission at the neuromuscular junction. The neurotoxin produced by the bacterium Clostridium botulinum irreversibly impedes the intracellular mechanisms responsible for the release of acetylcholine from the presynaptic nerve terminals.458

ETIOLOGY The different neurotoxins produced in botulism exhibit different clinical characteristics. Type E botulism is usually associated with eating seafood; pupillary abnormalities and ptosis may be seen as early signs. Gastrointestinal symptoms are more prevalent in type E and type B. The most severe form is type A, which carries the highest risk for ventilatory support and the highest mortality.

CLINICAL FEATURES Children may develop botulism from ingestion of contaminated food, wound infection, or intestinal infection in infants. Infants usually come to attention because of lethargy, weakness, feeding difﬁculty, a feeble cry, and constipation.240 Older children report nausea, vomiting, blurred vision, dysphagia, and pooling of secretions in the mouth, followed by generalized weakness and diplopia. In both groups, ophthalmologic ﬁndings are common and may include any type or degree of external ophthalmoplegia, dilated pupils that react poorly to light, and ptosis.485 In one outbreak of 27 patients in the U.K., the complaints were of blurred vision in 78%, drooping lids in 56%, and double vision in 30%. In this report, 11 of 14 (79%) of reviewed records revealed sixth nerve palsy and 13 of 14 (93%) revealed accommodative paresis, both of which were early ophthalmic signs. The severity of ophthalmoparesis was a good indicator of the overall severity and progression of disease. When there was ventilatory failure, it occurred 12 h after third cranial nerve palsy.457 In another report, it was noted that sixth cranial nerve palsy may be the initial neurological manifestation of type B botulism.485 In 8 of 11 (73%) of their patients diagnosed with third nerve palsy, respiratory insufﬁciency eventually ensued.

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Quivering eye movements on attempted saccades have also been observed and analyzed on eye movement recordings, consisting of hypometric saccades with subnormal and stuttering velocities.200

CLINICAL ASSESSMENT Because botulism may be difﬁcult to distinguish clinically from Guillain–Barre syndrome,241 pupillary ﬁndings, which are rare in Guillain–Barre, become particularly important. Botulism may also be mistaken for myasthenia gravis (again, the pupils are helpful; a Tensilon test may be falsely positive in mild forms of botulism457), sudden infant death syndrome, and hypothyroidism in infants. In infants, EMG is the primary means of diagnosis.241

TREATMENT Treatment is essentially supportive. Antitoxin has been shown only to shorten the duration of illness in type E botulism, but is considered in patients with botulism as soon as the diagnosis is suspected as it can only act before the toxin is irreversibly bound to its receptor. Adverse reactions to the antitoxin have been reported in up to 20% of patients. Guanidine, a drug that enhances release of acetylcholine from the presynaptic nerve terminal, has only a slight effect on limb and ocular muscles and no effect on respiratory muscles.457

PROGNOSIS Recovery does not occur until new neuromuscular junctions are established, a process that may take weeks to months. The mortality from this condition in the United States has been reported as 7.5%; this ﬁgure is higher in developing countries.457

DISORDERS OF THE EXTRAOCULAR MUSCLES Abnormal extraocular muscles may limit eye movements through decreased function or through restriction. The pattern of limitation may simulate neural and neuromuscular disorders

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FIGURE 12-13. Fibrosis of the extraocular muscles. Severe ptosis (right photo) and eyes ﬁxed in depression with minimal to no movement typical of severe ﬁbrosis of the extraocular muscles.

so closely that force ductions, special imaging (echography, CT, MRI), or even surgical exploration may be necessary for differentiation. These disorders may be either congenital or acquired. Congenital anomalies of the extraocular muscles include agenesis, duplication, abnormal origins and insertions, fascial anomalies, and ﬁbrous bands.297,500,508,509,529 Congenital absence of one or more extraocular muscles limits movement of the globe in the direction of action of the missing muscle(s) and may mimic a nerve palsy. Indeed, in one series of presumed congenital superior oblique palsies for which a superior oblique tuck was deemed necessary and attempted, 18% of the patients were found to have congenital absence of the superior oblique.201 Agenesis and other forms of maldevelopment of the extraocular muscles have long been recognized and associated with craniofacial anomalies.124,384 At times, certain extraocular muscles mechanically restrict eye movements from birth, for example, in the congenital ﬁbrosis syndrome (Fig. 12-13) or congenital Brown’s syndrome. Acquired disorders such as trauma, dysthyroid myopathy, acquired Brown’s syndrome, and orbital myositis may all cause weakness or restriction of extraocular muscles. Although investigation of these disorders requires careful attention to the history and systemic health of the child as well as local ocular and orbital signs, such advertence is frequently rewarded.

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DISORDERS OF NERVE AND MUSCLE Kearns–Sayre Syndrome (Chronic Progressive Ophthalmoplagia) CLINICAL FEATURES AND NATURAL HISTORY Ptosis and chronic progressive limitation of eye movements, usually without diplopia, are features of a variety of disorders. Among these, Kearns–Sayre syndrome (KSS) is singularly apt to come to attention in childhood, most often because of ocular signs. The triad of external ophthalmoplegia, heart block, and retinal pigmentary degeneration identiﬁed in the original description of KSS256 remains the cornerstone of diagnosis, although a multitude of associated signs have since been recognized (Table 12-8). The eye movements in KSS show gradually progressive limitation, which is usually symmetrical and affects all directions of gaze. Bell’s phenomenon and eye movement responses to caloric stimulation or head rotation are also slowly lost. Anticholinesterase agents do not improve the range of eye movements. Pupils remain normal. The lids are typically ptotic and often close weakly because of involvement of the orbicularis TABLE 12-8. Manifestations of Kearns–Sayre Syndrome. System

Findings

Cardinal features

Chronic progressive external ophthalmoplegia; degenerative pigmentary retinopathy; cardiac conduction defects/sudden death; no family history

Musculoskeletal

Short stature; “ragged-red” ﬁbers by light microscopy of muscle tissue; skeletal and dental anomalies

Neurological

Elevated CSF protein; deafness; vestibular dysfunction; cerebellar ataxia; “descending” myopathy of face and limbs; mild corticospinal tract signs; subnormal intelligence; demyelinating polyradiculopathy; slowed electroencephalogram; decreased ventilatory drive/sudden death; spongiform degeneration of cerebrum and brainstem

Endocrine

Diabetes mellitus; hypogonadism; hypoparathyroidism; growth hormone deﬁciency; adrenal dysfunction; hyperglycemic acidotic coma/death; elevated serum lactate and pyruvate

Other

Corneal edema; nephropathy

Source: Modiﬁed from Glaser JS, Bachynski BN. Infranuclear disorders of eye movement. In: Glaser JS (ed) Neuro-ophthalmology, 2nd edn. Philadelphia: Lippincott, 1990:402, with permission.166

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oculi. Indeed, generalized facial weakness is frequent and contributes to a typical facial appearance. Affected fundi demonstrate a diffuse pigmentary retinopathy that characteristically involves the posterior pole as well as the periphery and generally consists of a “salt-and-pepper” pattern of pigment clumping. Commonly both rod and cone function are reduced on electroretinography,341 and although it has been noted that only 40% of patients have decreased visual acuity or night blindness,54 photoreceptor function can diminish insidiously with time.

SYSTEMIC ASSOCIATIONS Cardiac conduction defects, a cardinal feature of KSS, can be heralded by an interval of enhanced conduction at the A-V node and may lead to death at any time.88,404 Other systemic associations include small stature, ataxia, deafness, raised cerebrospinal ﬂuid protein, diabetes, and hypoparathyroidism (see Table 12-8).

CLINICAL ASSESSMENT On any patient suspected of KSS, an electrocardiogram is performed. Abnormal blood lactate and pyruvate levels may be found. On skeletal muscle biopsy, “ragged-red ﬁbers” and abnormal mitochondria are expected. In diagnosing patients suspected of KSS but with an incomplete constellation of ﬁndings, analysis of muscle mtDNA to look for mitochondrial deletions may be more critical than mitochondrial morphological examination (see following).178 The brain MRI of patients with KSS may show normal or atrophied brain, but the characteristic ﬁnding is a combination of high-signal foci in subcortical cerebral white matter, brainstem, globus pallidus, or thalamus.92

ETIOLOGY A protracted and shifting debate over the etiology and nosology of KSS has continued for decades. Early on, chronic progressive external ophthalmoplegia (CPEO) was considered to be an isolated myopathy of the extraocular muscles, with occasional weakness of the extremities.260 However, many subsequent reports described CPEO in conjunction with multisystem disease, with KSS itself serving as a good example. When spongiform degeneration of the brainstem and cerebrum, which is observed on neuropathological examination of patients with

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KSS, was highlighted, the neural structures governing eye movements became suspect. Next, myopathological ﬁndings pointed investigators in yet a different direction. In CPEO, light microscopy of muscle preparations processed with the modiﬁed Gomori trichrome stain frequently demonstrates “ragged-red” muscle ﬁbers among normal extraocular muscle ﬁbers, orbicularis oculi ﬁbers, and, at times, other skeletal muscle ﬁbers. With electron microscopy, these ragged-red ﬁbers as well as other muscle ﬁbers demonstrate markedly abnormal mitochondria. In KSS, such abnormal mitochondria were detected in a variety of other tissues as well, including sweat glands,245 liver cells,174 and cerebellar neurons.438 Experimental infusion of a chemical that uncouples oxidative phosphorylation produced reversible ragged-red ﬁbers.318 This morphological evidence combined with biochemical abnormalities indicating mitochondrial dysfunction led to speculation about the role of mitochondrial DNA (mtDNA) in the pathogenesis of these disorders.

INHERITANCE The majority of KSS and CPEO cases are sporadic. In one review, only a single family demonstrated more than one person manifesting the entire KSS.420 When small pedigrees with multiple individuals exhibiting CPEO have been reported, transmission has generally been maternal and compatible with mitochondrial inheritance,140,223,236 but paternal transmission of CPEO has also been observed, suggesting a defective autosomal nuclear gene in some cases.139,140,467 New techniques in molecular biology have triggered an explosion of studies of mtDNA in patients with KSS and CPEO.178,334 A signiﬁcant proportion of these patients show large-scale heteroplasmic deletions in mtDNA, and these deletions play a pivotal role in the pathogenesis of these disorders. Heteroplasmy denotes the presence of several different mtDNA in a cell, some of which may be pathogenic. KSS and CPEO patients have heteroplasmy in different proportions depending on the tissue studied222: large-scale deletions of mtDNA have been observed in muscle of 80% of KSS patients and 70% of those with CPEO.178 Based on these observations, it has been suggested that CPEO and KSS are different severities along the same clinical spectrum.131,178 Another ﬁnding that may explain the overlap between the clinical presentations of KSS and CPEO is that patients with

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these two diseases have identical mtDNA deletions, but in KSS they are localized to the muscle and neural tissues, whereas in CPEO they are localized to muscle. Another disease called Pearson syndrome also has the identical deletions as in KSS and CPEO but is localized to the blood. In fact, patients with Pearson syndrome may develop KSS later in life. On the other hand, mtDNA duplications have been observed in KSS but not in CPEO patients,178 a difference that lends support to the idea that these are two distinct clinical entities, as suggested earlier.54 The severity of disease in patients with mitochondrial deletions apparently depends on a variety of factors: (1) the degree of heteroplasmy, or the distribution of normal and mutant mitochondria; (2) the nature of the mitochondrial mutation; (3) reduction in absolute amounts of normal mtDNA; and (4) a homoplasmic mutation that leads to a large deletion.178

TREATMENT AND PROGNOSIS The prognosis for patients with KSS is fair, and treatment is largely symptomatic. Patients can frequently be managed with a cardiac pacemaker382 to obviate conducting ﬁbers that, on pathological study, are ﬁbrotic and inﬁltrated by fat.156,160 Despite cardiac pacing, patients may die suddenly of inadequate brainstem ventilatory response to hypoxia.82,104 Abrupt and fatal endocrine dysfunction may also be triggered by steroids,38 and there can be hypersensitivity to agents used during induction of general anesthesia.233 For many pediatric patients, however, it is the relentless progression of neurological deﬁcits, especially weakness and ataxia, rather than the possibility of sudden demise, that proves to be particularly trying. Preliminary reports suggest that administration of coenzyme Q10, a quinone found in the mitochondrial oxidative system (with reported doses of 60–120 mg daily for 3 months in one patient,357 50 mg 3 times a day for 3 months in two others359), may improve A-V block as well as normalize serum pyruvate and lactate levels358; improve neurological function without an effect on the ophthalmoplegia or the electrocardiogram70; and increase respiratory vital capacity when used with succinate.452 Surgery is generally not recommended for either ptosis or strabismus in these patients as it is a progressive disease. Surgical correction of ptosis would involve a high risk of exposure

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keratopathy, especially because the eye will lose its Bell’s phenomenon during the course of the disease and corneal wetting would not occur. Diplopia from strabismus may be treated with prisms and, as a last resort, monocular occlusion.

Myotonic Dystrophy Myotonic dystrophy, also known as dystrophia myotonica or Steinert’s disease, is an autosomal dominant multisystem disorder with variable phenotype. Early investigators focused on muscle as the primary site of involvement; subsequent studies revealed that the nervous system231 as well as a variety of other tissues are affected in addition to the muscles. At least two main types of myotonic dystrophy exist, termed DM1 and DM2. Two other described forms, called proximal myotonic myopathy (PROMM) and proximal myotonic dystrophy (PDM), are closely linked to the DM2 locus and may be caused by the same genetic defect with different phenotypic expression.

INCIDENCE Myotonic dystrophy is considered as one of the most frequent “dystrophies” in adulthood, with a prevalence of approximately 5 in 100,000 in white European populations.401

ETIOLOGY The fascinating pathogenesis of DM1 has been described as a result of various mechanisms.319 The most important factor is the expanded trinucleotide cytosine-thymidine-guanine (CTG) repeats in the 3 -untranslated region of the disease gene, dystrophia myotonica protein kinase (DMPK) gene, which leads to decreased DMPK messenger RNA (mRNA) expression and protein levels. However, DMPK knockout mice showed only mild muscle weakness and abnormal cardiac conduction. On further investigation, it was found that the expanded trinucleotide repeat in the mRNA is toxic to the muscle, because when transgenic mice were developed that express human skeletal actin—unrelated to the DMPK gene—with expanded CTG repeats in the 3 -untranslated region, the mice developed myotonia and myopathy.304 A signiﬁcant correlation exists between age of onset and number of CTG repeats and a general correlation between the degree of CTG expansion and the severity of disease manifesta-

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tions. Mildly affected patients have 50 to 150 repeats, classic DM1 patients have 100 to 1000, and congenital cases may have more than 2000.319 The exact pathological mechanism remains unclear, but a theory unifying the protean manifestations of the disease has been proposed, namely that the fundamental defect is a generalized abnormality of cell membranes.418 Recent evidence supports the hypothesis that DMPK deﬁciency is associated with sodium channel abnormality in DM.336

CLINICAL FEATURES AND NATURAL HISTORY Unlike KSS, ocular motility abnormalities in myotonic dystrophy are commonly subclinical and have been observed for the most part in adults. A number of authors have described progressive limitation of voluntary eye movements as well as markedly decreased maximum saccadic velocity and reduced smooth pursuit gain, but it is not clear whether these eye movement disorders result from a neurological or myopathic defect or both.14,123,143,290,364,449,484,503 Clinical myotonia, that is, delayed muscular relaxation, most strikingly affects the limb muscles (e.g., persistent grip), but may on occasion involve the extraocular muscles134; immediately after sustaining gaze in a certain direction, the patient cannot promptly move the eyes in the opposite direction. Bell’s phenomenon is particularly useful to elicit sustained upgaze in an infant or uncooperative child. Although the manifestations of myotonic dystrophy usually become apparent in adolescents or young adults, detailed questioning often documents symptoms during the ﬁrst decade of life, and the disease can, at times, affect infants and young children distinctly.127 For the ophthalmologist, a characteristic facial appearance (facial diplegia, triangular-shaped mouth, and slack jaw) and weak orbicularis function typically without ptosis suggests the possibility of myotonic dystrophy in a young child. Bilateral facial weakness is the most characteristic feature of early-onset myotonic dystrophy and is frequently misdiagnosed as Möbius syndrome (see following section). With increasing age, the more familiar facial appearance of myotonic dystrophy (narrow, expressionless, “hatchet” face with hollowing of cheeks and temples) evolves because wasting of the facial muscles occurs, and ptosis becomes far more common. PROMM, PDM, and DM2 are also autosomal dominant myotonic dystrophy without the CTG repeat expansion at the

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DM1 locus. PROMM and PDM predominantly involve proximal muscles, and DM2 involves distal muscles. All three have been linked to chromosome 3q21.3 and may be various phenotypes of the same disease. These patients also develop posterior subcapsular cataracts with onset before 50 years of age. They do not exhibit ophthalmoplegia, however.320

CLINICAL ASSESSMENT Bilateral iridescent and posterior cortical lens opacities are useful for establishing a clinical diagnosis27; they may be identiﬁed in young children but are often not seen until the teenage years. Clear electroretinographic abnormalities with normalappearing fundi may be observed early on,69 and a subgroup of patients demonstrate visual loss and observable pigmentary retinopathy later in the course of the disease. Additional ophthalmic signs are listed in Table 12-9.37 A negative family history does not exclude the diagnosis because a parent with myotonic dystrophy may be affected so mildly as to be unaware of it.374 Careful evaluation of the parents can therefore prove helpful. Beside the slit lamp examination for cataracts, other primary diagnostic tests include DNA testing for an enlarged CTG repeat, examination for muscle and nonmuscle manifestations, and EMG for subclinical myotonia. Secondary tests include serum creatinine kinase, which is often mildly elevated in

TABLE 12-9. Ophthalmic Manifestations of Myotonic Dystrophy. Structure

Findings

Eyelids

Ptosis; myotonic lag (due to delayed relaxation of levator); orbicularis weakness; myotonic closure (due to delayed relaxation of orbicularis)

Motility

Slow saccades with full ductions and versions; myotonia induced by Bell’s reﬂex, convergence, or eccentric gaze; partial to complete ophthalmoplegia (usually symmetrical)

Globe

Cataracts (subcapsular polychromatophilic opacities; posterior cortical spokes; posterior subcapsular plaques; mature cataracts); short depigmented ciliary processes; hypotony; iris neovascular tufts (resulting in spontaneous hyphema); keratitis sicca; macular and peripheral retinal pigmentary degeneration; miotic, sluggishly reacting pupils

Miscellaneous

Decreased ERG responses; elevated dark-adaptation thresholds; generalized constriction of visual ﬁelds

Source: From Ref. 37, with permission.

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diseased individuals, and muscle biopsy, which frequently shows an increase in central nuclei, ﬁber atrophy, and ringed ﬁbers.

INHERITANCE The interesting feature of this disease is that when it is passed on from one generation to the next in autosomal dominant fashion, the severity of disease increases. The phenomenon of progressive earlier onset and greater severity of disease is termed anticipation; this is particularly true for cases of female transmission, which can lead to the congenital cases of the disease. Increased severity in the subsequent generations is associated with increased expansion of the CTG repeats.303 DM1 gene has been mapped to chromosome 19q13.3. DM2, PROMM, and PDM have all been linked to chromosome 3q21.3, but the gene defect(s) has not yet been identiﬁed.320

SYSTEMIC ASSOCIATIONS In addition to facial diplegia, infants frequently demonstrate hypotonia, delayed motor and intellectual development, feeding difﬁculties, neonatal respiratory distress, and talipes.192 In adults, diabetes, pituitary dysfunction, widespread involvement of the smooth muscle of the gastrointestinal tract, premature balding, and gonadal atrophy may all be seen.

TREATMENT AND PROGNOSIS Comprehensive medical care of patients with myotonic dystrophy is essential. Prompt intervention may become necessary at any time because of associated, potentially life-threatening, cardiac conduction defects. Periodic EKGs are obtained to detect heart block, which may require a pacemaker. Drugs such as procainamide, quinine, and propranolol are avoided in patients with cardiac involvement. Endocrinological management is necessary for those patients who also have diabetes or pituitary dysfunction. Prostheses may be used for foot and hand weakness. Myotonia may be moderately reduced with mexiletine and tocainide, which have been found to be more effective than phenytoin and dysopyramide. Any strabismus surgery for myotonic dystrophy patients is approached with caution because of the potential for friable and atrophic extraocular muscles.306 Also any ptosis surgery risks

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corneal exposure due to lack of Bell’s phenomenon in the setting of ophthalmoplegia. Life expectancy is reduced particularly in the case of early onset disease and proximal muscle involvement. The high mortality rate is due to an increase in deaths from respiratory diseases, cardiovascular diseases, and neoplasms, as well as sudden deaths from cardiac arrhythmias.320

Möbius Syndrome Möbius328,329 designated congenital, bilateral sixth and seventh nerve palsies as central features of what has come to be known as Möbius’ syndrome, but subsequent clinical and pathological observations reveal greater complexity. It has become clear that the eponym has been applied to a heterogeneous group of congenital neuromuscular disorders that produce facial weakness in some combination with a variety of other ﬁndings (Table 12-10). It has been suggested that the term sequence is more appropriate because a sequence deﬁnes a cascade of secondary events after an embryonic insult from heterogeneous causes.325

Clinical Features and Systemic Associations Typically, a short time after birth, an affected infant demonstrates difﬁculty feeding because of poor sucking and little, if TABLE 12-10. Manifestations of Möbius Syndrome. System

Findings

Cardinal features

Partial or complete facial paralysis, usually bilateral (may be unilateral)203,324 Straight eyes, esotropia, or exotropia with no horizontal movements and preserved vertical movements324,407,461; total ophthalmoplegia206,324,464; cocontraction of horizontal recti61 Unilateral or bilateral palsy of cranial nerves V, VIII, IX, X, or XII42,475; autism325 Abnormal tongue; biﬁd uvula; cleft lip/palate; micrognathia, microstomia; external ear defects324,325 Syndactyly; brachydactyly; absent or supranumerary digits; arthrogryposis multiplex congenital; talipes; absence of hands or feet324,325,409,461 Mental retardation325; congenital heart defects; absent sternal head of the pectoralis major (second major component of the Poland anomaly)324,325; rib defects; Klippel–Feil anomaly; neuroradiologic cerebellar hypoplasia51,190; hypogonadotropic hypogonadism with or without anosmia362,422

Ocular motor

Neurological Orofacial Musculoskeletal

Miscellaneous

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any, facial expression, as a result of the involvement of cranial nerves IX and XII in addition to VII. Generally, horizontal eye movements are clearly abnormal, and vertical eye movements are preserved. If convergence is intact and used for crossﬁxation, the ocular motility pattern may resemble that produced by bilateral sixth nerve palsies. On occasion, vertical eye movements may also be affected or total ophthalmoplegia may occur. Crocodile tears, micrognathia, dental anomalies, cleft palate, facial asymmetry, limb malformations, Poland’s syndrome, epilepsy, mental retardation, and autism may be present.325

Etiology Fifteen autopsied cases have been classiﬁed into four groups based on neuropathological ﬁndings in the brainstem.489 Group I demonstrated absence or hypoplasia of relevant cranial nerve nuclei; group II, in addition to neuronal loss, showed evidence of neuronal degeneration suggesting peripheral nerve injury; group III, in addition to neuronal loss and neuronal generation, had frank necrosis of the tegmentum of the lower pons; group IV revealed no abnormalities in the brainstem and may represent a purely myopathic disorder. Cases of facio-scapulohumeral muscular dystrophy and congenital centronuclear (myotubular) myopathy that clinically mimic Möbius syndrome would also presumably belong to group IV.189,199 A number of investigators have speculated that disruption of the vascular system causes hypoxia of vulnerable tissues between 4 and 7 weeks gestation.190,294,396 It has been proposed that Möbius syndrome, the Poland anomaly, and the Klippel–Feil defect all result from a transient interruption during the sixth week of gestation in the development of the subclavian artery and its branches, including the basilar, vertebral, and internal thoracic arteries, which supply the brain, neck, pectoral muscles, and upper limbs; in addition, in Möbius syndrome, the primitive trigeminal artery that supplies the hindbrain during fetal life may regress before the establishment of adequate perfusion from the vertebral or basilar artery and thereby disturb development of the cranial nerve nuclei.48 Such a mechanism would be consistent with the brainstem necrosis seen in group III Möbius’ syndrome patients but would not account for the ﬁndings in groups I and II.

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Inheritance As might be expected, most reported cases have been sporadic, and the sexes are affected with equal frequency. At least ﬁve families with Möbius’ syndrome have been reported without any one consistent chromosomal defect.206,283,325,531 Chromosomal translocations (1;13 and 1;11), chromosome 13q12.2 deletion, and linkage to chromosome 3q21–22 have been reported by previous authors. The recurrence risk to siblings of isolated cases with these three manifestations appears to be less than 2%.42

Treatment and Prognosis Depending on the severity and types of malformations, the treatment will vary.325 Initially, sucking problems often require modiﬁcation in type of bottle used. If lid lag is present from seventh nerve palsy, lubricants are necessary. Refractive errors, amblyopia, and strabismus often need attention. Maximal medial rectus recessions with or without vertical displacement have been shown to sufﬁce in some cases,466,516 whereas others have advocated horizontal recessresections321,346,490 or vertical muscle transposition.206,470 Because of the lack of facial expression, parents and children may have psychological difﬁculty with bonding and social communication. Plastic surgeries do exist that can improve facial movement.81,543 Finally, helping families cope by contacting others through a national organization, such as the Möbius Syndrome Foundation, is also important and appreciated, as is the case for other diseases or syndromes mentioned in this chapter.

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475. Sudarshan A, Goldie WD. The spectrum of congenital facial diplegia (Moebius syndrome). Pediatr Neurol 1985;1(3):180–184. 476. Sullivan S. Benign recurrent isolated VI nerve palsy of childhood. Clin Pediatr 1985;24:160–161. 477. Summers CG, MacDonald JT, Wirtschafter JD. Ocular motor apraxia associated with intracranial lipoma. J Pediatr Ophthalmol Strabismus 1987;24(5):267–269. 478. Swick HM. Pseudointernuclear ophthalmoplegia in acute idiopathic polyneuritis (Fisher’s syndrome). Am J Ophthalmol 1974;77(5):725– 728. 479. Sydnor CF, Seaber JH, Buckley EG. Traumatic superior oblique palsies. Ophthalmology 1982;89(2):134–138. 480. Tamura EE, Hoyt CS. Oculomotor consequences of intraventricular hemorrhages in premature infants. Arch Ophthalmol 1987;105(4): 533–535. 481. Taylor MJ, Polomeno RC. Further observations on the auditory brainstem response in Duane’s syndrome. Can J Ophthalmol 1983; 18(5):238–240. 482. Tekkok IH, et al. Bilateral intranuclear ophthalmoplegia associated with fourth ventricular dermoid tumor. J Clin Neuroophthalmol 1989;9(4):254–257. 483. Teller J, Karmon G, Savir H. Long-term follow-up of traumatic unilateral superior oblique palsy. Ann Ophthalmol 1988;20(11):424–425. 484. Ter Bruggen JP, et al. Disorders of eye movement in myotonic dystrophy. Brain 1990;113(pt 2):463–473. 485. Terranova W, Palumbo JN, Breman JG. Ocular ﬁndings in botulism type B. JAMA 1979;241(5):475–477. 486. Thomas R, et al. Bilateral synergistic divergence. J Pediatr Ophthalmol Strabismus 1993;30(2):122–123. 487. Tjissen C, Goor C, van Woerkom T. Spasm of the near reﬂex: functional or organic disorder? Neuro-Ophthalmology 1983;3:59–64. 488. Toshniwal P. Demyelinating optic neuropathy with Miller–Fisher syndrome. The case for overlap syndromes with central and peripheral demyelination. J Neurol 1987;234(5):353–358. 489. Towﬁghi J, et al. Mobius syndrome. Neuropathologic observations. Acta Neuropathol (Berl) 1979;48(1):11–17. 490. Traboulsi EI, Maumenee IH. Extraocular muscle aplasia in Moebius syndrome. J Pediatr Ophthalmol Strabismus 1986;23(3):120–122. 491. Tredici TD, von Noorden GK. Are anisometropia and amblyopia common in Duane’s syndrome? J Pediatr Ophthalmol Strabismus 1985;22(1):23–25. 492. Tripp JH, et al. Juvenile Gaucher’s disease with horizontal gaze palsy in three siblings. J Neurol Neurosurg Psychiatry 1977;40(5):470–478. 493. Trobe JD, Glaser JS, Post JD. Meningiomas and aneurysms of the cavernous sinus. Neuro-ophthalmologic features. Arch Ophthalmol 1978;96(3):457–467. 494. Trobe JD. Cyclodeviation in acquired vertical strabismus. Arch Ophthalmol 1984;102(5):717–720.

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495. Trobe JD. Third nerve palsy and the pupil. Footnotes to the rule. Arch Ophthalmol 1988;106(5):601–602. 496. Troost BT, et al. Upbeat nystagmus and internuclear ophthalmoplegia with brainstem glioma. Arch Neurol 1980;37(7):453–456. 497. Tsai L, et al. Oculomotor apraxia in a case of Gaucher’s disease with homozygous T1448C mutation. Chung Hua Min Kuo Hsiao Erh Ko I Hsueh Hui Tsa Chih 1996;37:52–55. 498. Vajsar J, et al. Arthrogryposis multiplex congenita due to congenital myasthenic syndrome. Pediatr Neurol 1995;12(3):237–241. 499. Valbuena O, et al. Ataxia telangiectasia: review of 13 new cases. Rev Neurol 1996;24(125):77–80. 500. Valmaggia C, Zaunbauer W, Gottlob I. Elevation deﬁcit caused by accessory extraocular muscle. Am J Ophthalmol 1996;121(4):444– 445. 501. Vassella F, Lutschg J, Mumenthaler M. Cogan’s congenital ocular motor apraxia in two successive generations. Dev Med Child Neurol 1972;14(6):788–796. 502. Velez FG, Clark RA, Demer JL. Facial asymmetry in superior oblique muscle palsy and pulley heterotopy. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(4):233–239. 503. Versino M, et al. Lateral gaze synkinesis on downward saccade attempts with paramedian thalamic and midbrain infarct. J Neurol Neurosurg Psychiatry 1999;67(5):696–697. 504. Victor DI. The diagnosis of congenital unilateral third-nerve palsy. Brain 1976;99(4):711–718. 505. Vincent C, et al. A proposed new contiguous gene syndrome on 8q consists of branchio-oto-renal (BOR) syndrome, Duane syndrome, a dominant form of hydrocephalus and trapeze aplasia; implications for the mapping of the BOR gene. Hum Mol Genet 1994;3(10): 1859–1866. 506. Vincent FM, Vincent T. Relapsing Fisher’s syndrome. J Neurol Neurosurg Psychiatry 1986;49(5):604–606. 507. Vivian A, Harris C, Kriss A. Oculomotor signs in infantile Gaucher disease. Neuro-Ophthalmology 1993;13:151–155. 508. von Ludinghausen M. Bilateral supernumerary rectus muscles of the orbit. Clin Anat 1998;11(4):271–277. 509. von Ludinghausen M, Miura M, Wurzler N. Variations and anomalies of the human orbital muscles. Surg Radiol Anat 1999;21(1): 69–76. 510. von Noorden GK, Murray E. Up- and downshoot in Duane’s retraction syndrome. J Pediatr Ophthalmol Strabismus 1986;23(5): 212–215. 511. von Noorden GK. A magnetic resonance imaging study of the upshoot-downshoot phenomenon of Duane’s retraction syndrome. Am J Ophthalmol 1991;112(3):358–359. 512. Wadia NH, Swami RK. A new form of heredo-familial spinocerebellar degeneration with slow eye movements (nine families). Brain 1971;94(2):359–374.

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513. Wadia NH, et al. A study of the neurological disorder associated with acute haemorrhagic conjunctivitis due to enterovirus 70. J Neurol Neurosurg Psychiatry 1983;46(7):599–610. 514. Wagner RS, Caputo AR, Frohman LP. Congenital unilateral adduction deﬁcit with simultaneous abduction. A variant of Duane’s retraction syndrome. Ophthalmology 1987;94(8):1049–1053. 515. Walsh F, Hoyt W. Clinical neuro-ophthalmology. Baltimore: Williams & Wilkins, 1969. 516. Waterhouse WJ, Enzenauer RW, Martyak AP. Successful strabismus surgery in a child with Moebius syndrome. Ann Ophthalmol 1993; 25(8):292–294. 517. Weeks CL, Hamed LM. Treatment of acute comitant esotropia in Chiari I malformation. Ophthalmology 1999;106(12):2368–2371. 518. Weinacht S, Huber A, Gottlob I. Vertical Duane’s retraction syndrome. Am J Ophthalmol 1996;122(3):447–449. 519. Weinberg DA, Lesser RL, Vollmer TL. Ocular myasthenia: a protean disorder. Surv Ophthalmol 1994;39(3):169–210. 520. Weintraub MI. External ophthalmoplegia, ataxia, and areﬂexia complicating acute infectious polyneuritis. Am J Ophthalmol 1977;83(3): 355–357. 521. Welch R. Chicken-pox and the Guillain–Barre syndrome. Arch Dis Child 1962;37:557–559. 522. Werner DB, Savino PJ, Schatz NJ. Benign recurrent sixth nerve palsies in childhood. Secondary to immunization or viral illness. Arch Ophthalmol 1983;101(4):607–608. 523. Whitsel EA, Castillo M, D’Cruz O. Cerebellar vermis and midbrain dysgenesis in oculomotor apraxia: MR ﬁndings. AJNR Am J Neuroradiol 1995;16(suppl 4):831–834. 524. Wieacker P, et al. A new X-linked syndrome with muscle atrophy, congenital contractures, and oculomotor apraxia. Am J Med Genet 1985;20(4):597–606. 525. Wilcox LM Jr, Gittinger JW Jr, Breinin GM. Congenital adduction palsy and synergistic divergence. Am J Ophthalmol 1981;91(1):1–7. 526. Williams AS, Hoyt CS. Acute comitant esotropia in children with brain tumors. Arch Ophthalmol 1989;107(3):376–378. 527. Willison HJ, O’Hanlon GM. The immunopathogenesis of Miller Fisher syndrome. J Neuroimmunol 1999;100(1–2):3–12. 528. Wilson ME, Hoxie J. Facial asymmetry in superior oblique muscle palsy. J Pediatr Ophthalmol Strabismus 1993;30(5):315–318. 529. Wilson RS, Landers JH. Anomalous duplication of inferior oblique muscle. Am J Ophthalmol 1982;93(4):521–522. 530. Wise GA, McQuillen MP. Transient neonatal myasthenia. Clinical and electromyographic studies. Arch Neurol 1970;22(6):556–565. 531. Wishnick M, et al. Mobius syndrome and limb abnormalities with dominant inheritance. Ophthalmic Pediatr Genet 1983;2:77–81. 532. Woods CG, Taylor AM. Ataxia telangiectasia in the British Isles: the clinical and laboratory features of 70 affected individuals. Q J Med 1992;82(298):169–179.

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533. Woody R, Reynolds J. Association of bilateral internuclear ophthalmoplegia and myelomeningocele with Arnold–Chiari malformation type II. J Clin Neuroophthalmol 1985;5:124–126. 534. Woody RC, Blaw ME. Ophthalmoplegic migraine in infancy. Clin Pediatr (Phila) 1986;25(2):82–84. 535. Wright PW, Strauss GH, Langford MP. Acute hemorrhagic conjunctivitis. Am Fam Physician 1992;45(1):173–178. 536. Wybar K. Disorders of ocular motility in brain stem lesions in children. Ann Ophthalmol 1971;3(6):645–647. 537. Yang MC, et al. Electrooculography and discriminant analysis in Duane’s syndrome and sixth-cranial-nerve palsy. Graefe’s Arch Clin Exp Ophthalmol 1991;229(1):52–56. 538. Yeh JH, et al. Miller Fisher syndrome with central involvement: successful treatment with plasmapheresis. Ther Apher 1999;3(1):69–71. 539. Yuki N. Pathogenesis of Guillain–Barre and Miller Fisher syndromes subsequent to Campylobacter jejuni enteritis. Jpn J Infect Dis 1999;52(3):99–105. 540. Zaret CR, Behrens MM, Eggers HM. Congenital ocular motor apraxia and brainstem tumor. Arch Ophthalmol 1980;98(2):328–330. 541. Zasorin NL, Yee RD, Baloh RW. Eye-movement abnormalities in ophthalmoplegia, ataxia, and areﬂexia (Fisher’s syndrome). Arch Ophthalmol 1985;103(1):55–58. 542. Zee DS, Yee RD, Singer HS. Congenital ocular motor apraxia. Brain 1977;100(3):581–599. 543. Zuker RM. Facial paralysis in children. Clin Plast Surg 1990;17(1): 95–99.

13 Optical Pearls and Pitfalls David L. Guyton, Joseph M. Miller, and Constance E. West

O

ptics and refraction are often thought of as a dry chapter in ophthalmology, but understanding a few basic principles enables one to avoid errors and complications when treating both pediatric and adult strabismic patients.

REFRACTION AND REFRACTIVE ERROR IN CHILDREN Retinoscopy need not be limited to preverbal children following cycloplegia. Dry retinoscopy is useful both in evaluating the ability to accommodate and in serving as a quick assessment of the present pair of glasses. To check the present correction, two free lenses, a 1.50 D and a 2.00 D, are grasped between the thumb and foreﬁnger of one hand and held in front of the two eyes. The patient is instructed to look at the distance ﬁxation target through the 2.00 D lens, thus relaxing accommodation. The eye being evaluated is then checked with the 1.50 D lens with the retinoscope on axis for neutrality. Dynamic retinoscopy, performed to evaluate the effectiveness of accommodation, is performed without free lenses. One eye of the subject is occluded. A ﬁxation target is held just below the peephole of the retinoscope, and the subject is instructed to look ﬁrst at a distance target, then at a near one. If the subject is able to focus on the near target, the observer will see neutralization of the retinoscopy reﬂex. This test is most useful in assessing the need for bifocal correction in an amblyopic eye. If the child cannot readily accommodate and neutralize the reﬂex at near, even if there is no element of accommodative esotropia, a reading add should be considered. Performing dynamic 520

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retinoscopy with both the patient’s eyes open provides a good screen for anisometropia or sphere imbalance in the glasses. Cycloplegic refraction is an essential part of the examination of strabismic children and may be effected by several drugs with different cycloplegic and mydriatic characteristics. The agents most commonly used by strabismologists are atropine, cyclopentolate, and tropicamide. Atropine blocks parasympathetic activity by competing with acetylcholine and therefore prevents contraction of the ciliary muscle and iris sphincter. Mydriasis is fully developed at 35 to 45 min, while cycloplegia is not completed until 1 h after instillation of eyedrops. Atropine has the longest duration of cycloplegia (up to 48 h) and mydriasis (up to several days) of the parasympatholytic drugs. Tropicamide 1% is a short-acting (3–6 h duration) mydriatic with a rapid onset of cycloplegia (20–30 min). Cyclopentolate, like tropicamide, is a synthetic parasympatholytic but seems to be a more effective cycloplegic with peak accommodative paresis between 25 and 35 min. Its mydriatic action may last for 24 h. One cannot measure accommodative amplitude, reading adds cannot be determined, and strabismic deviations are affected after the administration of cycloplegic agents. The authors’ preferred practice with children is to anesthetize the conjunctiva with a topical anesthetic, followed by instillation of 1% cyclopentolate. The anesthetic seems to lessen the discomfort caused by the cyclopentolate and has the advantage of increasing its penetration into the anterior chamber. Cyclomydril (cyclopentolate 0.2% and phenylephrine hydrochloride 0.5%) or 0.5% cyclopentolate should be used in neonates and infants. In adults who require a cycloplegic refraction, we use 1% tropicamide because of its shorter duration of cycloplegia. When adequate cycloplegia cannot be effected in the ofﬁce (usually in children with darkly pigmented irises), prescribe atropine sulfate 1%, one drop in each eye, morning and evening for 2 days before the next visit. On the day of the visit, a drop should be instilled in each eye 1 h before the appointment. Local allergic (hypersensitivity) reactions manifested by conjunctivitis, swollen lids, and periocular dermatitis are occasionally seen with atropine administration but rarely, if ever, with tropicamide or cyclopentolate. All cycloplegic medicines have potential systemic side effects: ﬂushing, fever, dry skin and mucous membranes, tachycardia, restlessness, hallucinations, seizures, and even death, especially in the smallest and most

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lightly pigmented children. Severe reactions are rare but may require administration of intravenous physostigmine (0.5– 1.0 mg in children, 1–4 mg in adults, administered as a 0.2 mg/ml solution over at least 2 min). Systemic side effects may be lessened by occluding the canaliculi and preventing absorption by the nasal mucosa. Special care must be taken when atropine is given for administration at home, where the dose given is less controlled than in the ofﬁce. One 50-␮l drop of 1% atropine sulfate contains 0.5 mg of atropine, whereas the dose of atropine in resuscitation of the infant and child is 0.01 to 0.03 mg/kg! Be particularly careful in small babies and children with heart disease. Most neonates (approximately 75%) are hyperopic.2 The hyperopia is usually symmetrical and less than 4 D.8 It is also known that the degree of hyperopia usually increases until about the age of 7 years.1 The increase in hyperopia during early childhood also seems to apply to neonates born myopic and results in loss of myopia in those neonates born with a small amount of myopia.5 Thus, the majority of children examined have some degree of refractive error.

PRESCRIBING GUIDELINES AND LENS TYPES Once the refractive error has been determined, a decision must be made about whether to give the correction. In the absence of strabismus, the decision as to when to prescribe the correction must be made based on the magnitude of the error, the patient’s ability to accommodate, the visual needs of the individual, and the risk of refractive and/or anisometropic amblyopia. There are few data regarding who should receive glasses, but some common sense and general guidelines are helpful. Myopic children should receive correction when their uncorrected binocular visual acuity is 20/30 or worse. This level of acuity frequently occurs at 1.50 D in both eyes and is the threshold to follow for simple, symmetrical myopia. Hyperopia has no such simple guideline, as there is a tremendous variation in how children respond to an accommodative demand. Many children will not accommodate consistently at a level above 5.00 D and will require at least partial correction to allow for normal visual development. For high hyperopia, which is usually accompanied by subnormal accommodation, prescribe

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the full hyperopic correction (perhaps cut by 0.50 D), especially when there is abnormal visual function. It is a little easier to determine when to prescribe glasses in the presence of anisometropia. If both eyes are developing normal visual acuity and normal binocular function is present, no glasses are given. However, if anisometropic amblyopia is present (usually in the more ametropic eye), glasses must be prescribed. In anisometropic hyperopic amblyopia, the full correction need not be prescribed so long as the correction is reduced equally in each eye. In anisometropic myopic amblyopia, the full correction should be given. Pay careful attention to accommodative abilities when children are forced to ﬁx with an amblyopic eye. A reading add may hasten treatment of the amblyopia during occlusion or atropine penalization therapy, although this has not been proven conclusively. If glasses are to be prescribed for a signiﬁcant spherical error, any astigmatic error should be corrected as well. Astigmatic correction is given by itself when the child is not developing normal visual acuity; this usually occurs with 1.50 D or more of astigmatism. Children readily accept the full cylindrical correction at the proper axis, and it should be prescribed as such (not always the case with adults). Strabismus surgery can affect the refractive error, particularly the astigmatic component, and refraction should be rechecked after strabismus surgery. In the presence of high refractive errors, it is best to overrefract the individual and then read the resultant correction by placing both the free lenses and the glasses in a lensometer. Errors induced by changes in pantoscopic tilt or vertex distance will be eliminated. When strabismus coexists with a refractive error or an abnormal accommodative convergence/accommodation ratio, the full cycloplegic refraction should be given, adding bifocals if an esodeviation is still present at near. If alignment is not attained or maintained with spectacle correction, surgery may be considered. Bifocals, when used for the treatment of accommodative esotropia with a high accommodative convergence/ accommodation ratio, should be ﬁt high, usually with the top of the segment bisecting the pupil. Executive-style bifocals are commonly prescribed, but large, “D”-shaped (ﬂat-top) segments are frequently less expensive, lighter in weight, and provide adequate ﬁeld in pediatric patient frames. Progressive style bifocals have been advocated by some authors,3 but one should remember that the transitional zone is usually 12 mm in vertical extent

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and may render the most powerful part of the segment useless to pediatric patients. It is often prudent to specify a lens with high impact resistance (polycarbonate) for monocular and amblyopic children; special recreation spectacles are particularly appropriate for this population. Lens coating and ﬁlters are sometimes included in children’s corrective lenses. Ultraviolet protection should be considered for children with aphakia, lens implants, or maculopathy and for those children undergoing atropine penalization. Tinted and photochromic lenses, both of which are now available in glass or plastic, often provide comfort for patients with aniridia, ocular albinism, or oculocutaneous albinism.

THE CORNEAL LIGHT REFLEX AND STRABISMUS The corneal light reﬂex (the ﬁrst Purkinje–Sanson image) is a virtual image located 4 mm behind the cornea and may be thought of as located on an imaginary string connecting the center of curvature of the cornea with the ﬁxation light. To avoid errors from parallax in the Hirschberg or Krimsky4 test, the examiner’s eye must be directly behind the ﬁxation light. To produce Hirschberg test photographs of strabismic patients, the electronic ﬂash should be held directly below, or above, the camera lens, with a ﬁxation object placed between the ﬂash and the lens. Reﬂection of the camera ﬂash in the patient’s glasses can be detected by a handlight before taking the photograph and avoided by raising the temples, thus increasing the pantoscopic tilt of the glasses.

MEASUREMENT AND CORRECTION OF STRABISMIC DEVIATIONS WITH PRISMS Misalignment of the visual axes may be measured in degrees or prism diopters (PD). While strabismic deviations are measured in degrees in Europe, it is more common to quantify them in PD in the United States. Glass and plastic prisms are made with nonparallel surfaces that deviate light rays passing through them. The power of a prism (glass or plastic) in PD () is equal to the displacement, in centimeters, of a light ray passing through the prism, measured 100 cm from the prism (Fig. 13-1).

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FIGURE 13-1. A 15 prism displaces a light ray 15 cm when measured 100 cm from the plane.

Remember, when converting PD to degrees, that each degree is not exactly equal to 2 ; the relationship is a trigonometric one (degrees tan1(/100). For amounts less than 45° (100 ), the relationship of 2 per degree is roughly correct but, beyond 45° (100 ), the number of PD per degree increases rapidly without bounds, rising to an inﬁnite number of PD at 90°. Variability in strabismus surgery may result, in part, from incorrect use of prisms when measuring strabismic deviations preoperatively. Knowledge of these potential errors helps the ophthalmologist minimize their effects. These errors occur when prisms are incorrectly positioned or stacked in the same direction and when measuring deviations through high minus and high plus lenses. Ophthalmic prisms are made of either glass or plastic, and the amount of strabismic deviation neutralized (or produced) by the prism varies with the position in which it is held. There are three commonly used positions for holding ophthalmic prisms: Prentice position, minimum deviation position, and frontal plane position (Fig. 13-2). Glass prisms are calibrated for use in the Prentice position, which requires the patient’s line of sight to strike the rear (or front) surface of the prism at right angles. Small errors in holding glass prisms may produce large errors in the amount of deviation neutralized. For example, if the rear surface of a 40 glass prism is held in the frontal plane rather than in the Prentice position, the effect is only 32 .9 Plastic prisms and prisms bars are calibrated for use in the position of minimum deviation and, in this position, the line of

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FIGURE 13-2. The three common positions for use of ophthalmic prisms with ﬁxation at a distance: left, Prentice position; center, minimum deviation position; right, frontal plane position at distance (solid lines) and near (dashed lines). Plastic prisms should be held in the frontal plane position, and glass prisms are calibrated to be held in the Prentice position.

sight makes an equal angle with each of the faces of the prism. In clinical practice, however, the position of minimum deviation may be difﬁcult to judge. Holding the rear surface of the prism in the frontal plane of the patient very nearly produces the minimum deviation for that prism. Note, however, that if the rear surface of a 40 plastic prism is held in the Prentice position (a large error in holding a plastic prism) rather than in the frontal plane, the effect is 72 rather than 40 . Small errors in holding plastic prisms (in the frontal plane position instead of the minimum deviation position) produce only small errors in the amount of deviation neutralized. Thus, plastic prisms are less prone to position error than glass prisms and are preferable for this reason. The common practice of “stacking” two prisms together in the same direction to measure large deviations (greater than 50 ) may induce large errors. Glass prisms are available to a maximum of 40 and plastic prisms are available to a maximum of 50 . Prisms do not add linearly when stacked together in the same direction and should never be stacked together in that manner. Even though the rear surface of one of the prisms may be held in the correct position, the other prism is far from its calibrated position, and a much greater effect is produced than anticipated. For instance, a 3 plastic prism added to a 50 plastic prism gives a 58 effect.9 When measuring large deviations, prisms are best held before both eyes, although there is

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still some additivity error in doing this. The additivity errors induced have been tabulated by Thompson and Guyton9 or may be calculated with a formula. Fortunately, additivity error is not signiﬁcant when adding a vertical prism to a horizontal one. Thus, a vertical and a horizontal prism may be stacked together with no signiﬁcant interaction between the two when measuring a combined horizontal and vertical deviation. When measuring strabismic deviations with a ﬁxation target at near, the distance from the eye to the prism must be acknowledged. The amount of prism necessary to neutralize a deviation at near ﬁxation increases as the prism is held farther away from the eye; this effect may lead to overcorrections when the surgery is calculated on the basis of the near deviation.10 An additional error may result when measuring strabismic deviations through glasses, even when prisms are held in the proper position.7 This error is also present when measuring the deviation by the Krimsky prism reﬂex test or subjective methods. Both lines of sight of a strabismic patient cannot pass through the optical centers of the respective spectacle lenses; thus, glasses produce a prismatic change of the deviation as measured in front of the glasses. This peripheral prismatic effect begins to become clinically signiﬁcant with spectacle lenses of more than 5 D (minus or plus). Minus lenses increase the measured angle of deviation, and plus lenses decrease the measured angle, whether the deviation is esotropia, exotropia, or hypertropia. The distance deviation is changed by approximately (2.5) (D)%, where D is the spectacle power. For example, a 10 D bilateral high myope with 40 of exotropia will measure (2.5) (10)% more than 40 , or 50 , through the glasses. A helpful mnemonic is “minus measures more.” When calculating and prescribing oblique prisms, remember that prisms add as ordinary vectors, so a horizontal prism may be combined with a vertical prism and prescribed as a single prism at an oblique angle. The power and orientation of the prism may be determined by using a prism nomogram (Fig. 13-3), or by marking off proportional distances from the corner of a piece of paper, forming two sides of a right triangle. The third side of the triangle is proportional to the amount of oblique prism needed, and the orientation can be determined by folding the paper and measuring the appropriate angle with the protractor on a trial frame. The orientation of the prism base should be speciﬁed in the appropriate meridian, but note that over the left eye, for example, “base in the 135° meridian” is ambiguous.

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PR IS

M

RO

T IO AT N G AN

LE

FIGURE 13-3. Prism nomograph. To use the nomograph, determine the amount of vertical and horizontal prism needed to neutralize the deviation and then locate their intersection on the nomograph. The quarter circle nearest their intersection is the power of the prism to be used. Locate the intersection of this quarter circle and the amount of vertical prism determined on prism and cover test. A line drawn through this point and the origin intersects the prism rotation angle scale and determines the proper orientation of the oblique prism.

The base must be speciﬁed either as “base up and in at the 135° meridian” or as “base down and out in the 135° meridian.” Horizontal, vertical, or oblique prisms may be ground into spectacle correction, or Fresnel Press-On prisms may be applied to existing lenses. When one measures incomitant deviations with the prism and cover test,6 the deviation should always be neutralized with the prisms placed before each eye in turn. Only the eye not looking through the prism is truly pointing in the desired direction of gaze during testing. In this case, therefore, the “ﬁxing eye” must be deﬁned as the eye not looking through the prism;

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the position of the cover makes no difference. Once an incomitant deviation is neutralized with prism(s), no movement of either eye should be seen on movement of the cover from one eye to the other, unless a dissociated horizontal or vertical deviation is also present. When determining the amount of prism ground into, applied to, or caused by decentration (intentional or unintentional) of spectacles, it is important to measure the effective prism in the part of the lens through which the patient is looking. While the patient is looking through the spectacles, mark that point with the edge of a piece of paper tape. Then, measure the amount and orientation of the prism by placing this mark in the center of the nosecone of the lensometer.

References 1. Brown EVL. Net average yearly change in refraction of atropinized eyes from birth to beyond middle age. Arch Ophthalmol 1938;19: 719–734. 2. Cook RC, Glasscock RE. Refractive and ocular ﬁndings in the newborn. Am J Ophthalmol 1951;34:1407–1412. 3. Jacob J-L, Beaulieu Y, Brunet E. Progressive addition lenses in the management of esotropia with a high accommodation/convergence ratio. Can J Ophthalmol 1980;15:166–169. 4. Krimsky E. Fixational corneal light reﬂexes as an aid in binocular investigation. Arch Ophthalmol 1943;30:505–521. 5. Mohindra I, Held R. Refractions in humans from birth to 5 years. In: Fledelius HC, Alsbirk PH, Goldschmidt E (eds) Documenta Ophthalmologica Proceeding Series, vol 28. The Hague: Junk, 1981. 6. Repka MX, Kelman S, Guyton DL. Prism measurement of incomitant strabismus. Binoc Vis 1985;1:45–49. 7. Scattergood KD, Brown MH, Guyton DL. Artifacts introduced by spectacle lenses in the measurement of strabismic deviations. Am J Ophthalmol 1983;96:439–448. 8. Slataper FJ. Age norms of refraction and vision. Arch Ophthalmol 1950;43:466–481. 9. Thompson JT, Guyton DL. Ophthalmic prisms: measurement errors and how to minimize them. Ophthalmology 1983;90:204–210. 10. Thompson JT, Guyton DL. Ophthalmic prisms: deviant behavior at near. Ophthalmology 1985;92:684–690.

Index A Abduction deﬁcits of in Duane’s syndrome, 356, 357, 358, 359, 361 in infantile/congenital esotropia, 226, 227 in Möbius syndrome, 364–365 deﬁnition of, 27 AC/A ratio. See Accommodative convergence Accommodation in convergence, 99 deﬁciency of, 280 deﬁnition of, 161 normal development of, 7 relationship with convergence, 161 retinoscopic evaluation of, 520–521 Accommodative convergence (AC/A ratio), 99, 161–164 deﬁnition of, 161 in esotropia, 99 in accommodative esotropia, 243, 246–247 in exotropia, 99 in intermittent exotropia, 269, 271, 272, 275 with true divergence excess, 271, 272, 275 measurement of, 161–164 heterophoria method, 161–162 lens gradient method, 161–162, 163–164 Accommodative insufﬁciency, 280 Accommodative near targets, 3 Active forced-generation test, 169, 170, 171–172

Adduction deﬁcits of in Brown’s syndrome, 306, 315, 316 differential diagnosis of, 306, 316 in Duane’s syndrome, 356–357, 358, 359, 360, 361, 362 deﬁnition of, 27 Adhesive syndrome, 334 Adie’s pupil, as accommodative insufﬁciency cause, 280 Adjustable suture technique, 394–396 Afterimage test, 209–212 Albinism ocular, congenital exotropia associated with, 281 oculocutaneous, Duane’s syndrome-related, 359 Alcohol use, exotropia-inducing effect of, 266 Alcon Corporation, 17 Allen picture cards, 3, 11, 118, 141 Amblyopia, 108–125 ametropic (bilateral hypermetropic), 115–116 anisometropic, 114–115 myopic, lens-based correction of, 523 part-time occlusion therapy for, 130 astigmatic, 113, 114 bilateral meridional, 116 binocular ﬁxation preference testing in, 8 classiﬁcation of, 114 bilateral blurred retinal image, 110, 115–116 strabismic, 84, 110

531

532

index

Amblyopia (Continued) unilateral pattern distortion, 110, 113, 115 congenital exotropia-related, 281 cortical suppression in, 107, 109 cranial nerve III palsy-related, 442 cranial nerve VI palsy-related, 446 deﬁnition of, 108–109 diagnosis of, 7–11, 118–125, 140–141 with ﬁxation testing, 119–122 with vertical prism testing, 122–125 with visual acuity testing, 118 dissociated vertical deviationrelated, 373 Duane’s syndrome-related, 360–361 esotropia associated with, 223 ex anopsia, 109 extrafoveal ﬁxation associated with, 117 functional, 109 hypermetropic, 114, 115 bilateral, 115–116 intermittent exotropia surgeryrelated, 274 lateral geniculate nucleus (LGN) in, 110, 111, 190 Marcus Gunn jaw-winking-related, 468–469 monoﬁxation syndrome-related, 182 myopic, 115 occlusion therapy for, effect on contrast sensitivity, 14 organic, 109 pathology of, 109–110 pattern distortion in, 109 unilateral, 110, 113, 114, 115 prevalence of, 108 prognosis for, 133 reverse penalization-related, 131 prevention of, 130 stereopsis in, 114 strabismic, 84, 110 testing for, 116 treatment of, 127–133 for clear retinal image, 127, 128 ocular dominance correction in, 130–133 Amblyoscope, use in haploscopic tests, 204, 205–209

American Optical Hardy-Rand-Rittler (AO-HRR) plates, 13 Amniotic membrane transplantation, 334 Amputation defects, Möbius syndromerelated, 364 Anencephaly, extraocular muscle aplasia-related, 365 Anesthesia. See also Sedation physical examination under, 5 Angiography, of the iris, 59, 60 Angle kappa, 145–149 differentiated from tropias, 149 negative, 147 positive, 146–147, 148 physiological, 149 Anisekonia, 177 Anisometropia as anisekonia cause, 177 astigmatic, 127, 128 dynamic retinoscopic evaluation of, 520–521 hypermetropic, 127, 128 lens-based correction of, 523 Marcus Gunn jaw-winking-related, 468–469 myopic, 127, 128 red reﬂex test in, 128, 129 Anomalous retinal correspondence. See Retinal correspondence, anomalous (ARC) Anteriorization (anterior transposition), inferior oblique, 45–47, 311–312, 407–410 as dissociated vertical deviation treatment, 373 graded anteriorization technique of, 47 J-deformity associated with, 46–47, 312, 409, 410 as ocular restriction cause, 46–47, 327 Anterior segment ischemia of, 59–60, 354, 406 vascular supply to, 58–60 Anterior segment procedures, medial rectus muscle damage during, 34 Antiacetylcholine drugs, as myasthenia gravis cause, 470, 471, 475–476 Antiarrhythmic drugs, as myasthenia gravis cause, 472 Antibiotics, as myasthenia gravis cause, 472

index Anticholinesterase drugs, as myasthenia gravis cause, 472 Anticonvulsant drugs, as myasthenia gravis cause, 472 Antisaccades, 425 Antisuppression therapy as diplopia cause, 273 as horror fusionis cause, 189–190 Aphakia, ultraviolet protection in, 524 ARIX gene mutations, 339–340 Arnold-Chiari malformations, 431, 441 Asthenopia convergence insufﬁciency-related, 277, 280 intermittent exotropia-related, 267 Astigmatism bilateral, 116, 127, 128 corneal, 17 lens-based correction of, 523 Atropine, as cycloplegic agent, 18, 19, 172, 244, 521 contraindications to, 18 dosage of, 522 side effects of, 521 use in heart disease patients, 522 Atropine penalization, 130–131, 523 ultraviolet protection during, 524 Autorefractors, 20 Axes of Fick, 61 B Bagolini striated lens test, 179–180, 181, 184, 185, 190, 202–203 Bell’s palsy, recurrent, 459 Bell’s phenomenon, 4, 16–17, 431 in cranial nerve III palsy, 364 in dorsal midbrain syndrome, 436 in double elevator syndrome, 439 in Kearns-Sayre syndrome, 481, 484–485 in myotonic dystrophy, 486 Bielschowsky head tilt test, 65 Bifocals for accommodative esotropia, 523–524 for high-accommodative convergence esotropia, 247 Bifoveal vision (biﬁxation), 81 Binocular cortical cells, 70 Binocular eye movements, yoke muscles in, 64

533

Binocular fusion in Duane’s syndrome, 358, 359 head posturing associated with, 139 in horror fusionis, 188–190 Binocular sensory testing, 139 Binocular vision deﬁnition of, 70 development of, 104–105 cortical suppression-related abnormality in, 107 infantile esotropia-related impairment of, 220 motor fusion in, 70, 81–83 sensory fusion in, 70–83 binocular cortical cells in, 70, 71 corresponding retinal points in, 70–71 deﬁnition of, 70 disparate images in, 72 empirical horopter in, 71, 72, 73, 74–75 noncorresponding retinal points in, 72, 73 Panum’s fusional area in, 72, 73, 74 stereoacuity testing in, 76–80 stereoscopic vision in, 72, 74–75 Vieth-Müller circle in, 71, 72 Blebs, pseudo-Brown’s syndromerelated, 349, 350 Blepharoptosis, congenital ﬁbrosis of the extraocular muscles-related, 339 Blindness. See also Visual loss/ impairment unilateral, as sensory esotropia cause, 261–262 Blinking, “synkinetic,” 433–434 Blink response, normal development of, 7 Blurred vision convergence insufﬁciency-related, 277, 280 intermittent exotropia-related, 267 Botulinum toxin, 419–420 as cranial nerve VI palsy treatment, 446 as intrafacial synkinesis treatment, 469 Botulism, 478–479 Brain lesions. See also Brainstem tumors; Brain tumors contrast sensitivity in, 14

534

index

Brainstem anomalies of, as neural integrator abnormality cause, 431 lacunar infarcts of, 302 role in eye movements, 430 in saccadic eye movements, 427, 428, 437 Brainstem tumors as internuclear ophthalmoplegia cause, 441 as saccade initiation cause, 434 Brain tumors as cranial nerve VI palsy cause, 352 as esotropia cause, 445 as eye movement disorder cause, 431 as superior oblique paresis cause, 302 Break point, 278 Bridle-effect theory, of Duane’s syndrome, 147–148 Brown’s syndrome, 312–319 acquired, 312, 314, 315–316 idiopathic, 315, 316 inﬂammatory, 315, 316 as ocular restriction cause, 326 as “canine tooth syndrome,” 319 classiﬁcation of, 312, 314 clinical features of, 314–315 congenital (“true”), 312, 313, 314–315, 316–319 as ocular restriction cause, 326 surgical treatment of, 317–319 differentiated from inferior oblique paresis, 305, 306 monocular elevation deﬁcit syndrome, 341 primary superior oblique overaction, 306, 307 etiology of, 312–314 iatrogenic, 303–304, 412, 413 limited elevation in adduction associated with, 314–315 pseudo-, 327 surgical treatment of, 414, 416 Y-pattern strabismus associated with, 285 Brückner reﬂex test, 15, 149–150 in accommodative esotropia, 249 corneal light reﬂex in, 126, 127 in Duane’s syndrome, 358 in manifest latent nystagmus, 258 red reﬂex in, 126, 127

C Calipers, 3 Campylobacter jejuni infections, 457–458, 459 CAM therapy, for amblyopic eyes, 133 Cancer. See also speciﬁc types of cancer myasthenia gravis associated with, 476 “Canine tooth syndrome,” 319 Capsulopalpebral fascia, 36–37, 38–39 Cataracts congenital, early detection and treatment of, 125, 127, 128 effect on red reﬂex test, 126–127 unilateral as horror fusionis cause, 188–189 as sensory exotropia cause, 281 Caudal pons, role in saccadic eye movements, 429, 438 Central ﬁxation, as visual development milestone, 106–107 Central nervous system malformations of, saccade initiation failure associated with, 434 motility disorders of, 423–470 anomalies of innervation, 460–467 internuclear ophthalmoplegia, 440–441 ocular motor cranial nerve palsies, 442–470 supranuclear disorders, 432–440 Central nervous system depressants, phoria-inducing effect of, 85 Cerebellitis, as cranial nerve VI palsy cause, 443 Cerebellum anomalies of, as neural integrator abnormality cause, 431 role in eye movements, 430 Cerebral palsy, congenital exotropia associated with, 281 Check ligaments, 54, 57–58 Chin depression, 373–374, 375 surgical treatment of, 378 Chin elevation, 373–374 Brown’s syndrome-related, 315 monocular deﬁcit syndromerelated, 341

index Chin elevation (Continued) ptosis-related, 374, 378–379 surgical treatment of, 378 Chloral hydrate, 4, 5, 17 Chronic progressive external ophthalmoplegia (CPEO), 482–483 Cianci’s syndrome, 228–231, 232, 237, 256 Ciliary arteries, anterior and posterior, 58–58 in muscle transposition surgery, 404, 406 City University Color Vision Test (TCU test), 13 Clefts, oral or facial, Möbius syndromerelated, 364 Clinical distance-near relationship, 164 Clostridium botulinum, 478 Club foot, Möbius syndrome-related, 364 Coenzyme Q10, as Kearns-Sayre syndrome treatment, 484 Cogan’s lid switch sign, 474 Collicular plate sign, 435 Collier’s sign, 436 Color vision assessment, 12–13 Confusion, visual, 81, 177–178 deﬁnition of, 349, 351 glaucoma-related, 349, 351 Congenital Esotropia Observational Study (CEOS), 221–225, 228, 233 Congenital ﬁbrosis of the extraocular muscles (CFEOM), 339–340 Congenital ﬁbrosis syndrome, 231–232, 237 differentiated from infantile/ congenital esotropia, 219, 220 as ocular restriction cause, 325, 326 Conjunctivitis, acute hemorrhagic, 459–460 Contact lens, occlusive, as amblyopia treatment, 131 Contour stereoacuity test, 77, 78–80 monocular clues in, 78–79 Contrast dyes, as myasthenia gravis cause, 472 Contrast sensitivity, assessment of, 13–14 Contrast sensitivity function, 14 Contrast sensitivity threshold, 13–14 Convergence, 82–83 accommodative. See Accommodative convergence (AC/A ratio)

535

fusional, 95, 98 tonic, 99 normal amplitude of, 96 proximal or instrument, 100 relationship with accommodation, 161 interpupillary distance, 161 voluntary, 99 Convergence exercises, for convergence insufﬁciency, 278–279 Convergence insufﬁciency, 277–280 Convergence spasm, 439–440 Cornea, shape of, assessment of, 17 Corneal light reﬂex, 524 Corneal light reﬂex test. See Hirschberg test Corneal-pupillary axis, angle kappa of, 145–149 Cortical and basal ganglia dysplasia, 339 Cortical suppression in amblyopia, 107, 109 deﬁnition of, 84 as saccadic omission, 30 in sensory adaptations to strabismus, 178 Worth 4-dot test in, 199 Cover tests, 4, 150–159, 528–529 alternate cover test, 152–153, 154, 157 for cardinal positions of gaze measurement, 155 cover/uncover test, 149, 150–152, 154 interpretation of, 152, 154 prism alternate cover test, 154 simultaneous prism cover test, 155–157 variable measurements in, 154–155 Cranial nerve(s) palsies of, 442–460 combined, 456–457 general considerations in, 456–457 paresis of, 323–324 Cranial nerve III anomalies of, 462–463, 467–468 Marcus Gunn jaw-winking, 468–469 oculomotor synkinesis, 467 vertical retraction syndrome, 467–468 congenital ﬁbrosis of the extraocular muscles-related abnormalities of, 340

536

index

Cranial nerve III (Continued) in Duane’s syndrome, 355, 359 as inferior oblique muscle innervation, 45 as inferior rectus muscle innervation, 36 as medial rectus muscle innervation, 34 palsies of, 362–364, 452–456 amblyopia associated with, 442 congenital, 363–364, 454–455 with cyclic spasms, 455 partial, 453 traumatic, 453, 454, 456 treatment of, 363–364 role in eye movements, 424–425 in supranuclear eye movements, 427, 428 as superior rectus muscle innervation, 36 Cranial nerve IV congenital ﬁbrosis of the extraocular muscles-related abnormalities of, 340 palsies of, 446–452 superior oblique, 446–447, 449–450, 451 traumatic, 451–452 role in eye movements, 424–425 in supranuclear eye movements, 427 as superior oblique muscle innervation, 42 in traumatic superior oblique paresis, 299–300 Cranial nerve V, palsies of, 459–460 Cranial nerve VI agenesis of, as Duane’s syndrome cause, 355, 356–357 anomalies of, 460–467 in Duane’s syndrome, 460–466 in synergistic divergence, 466–467 immaturity of, as infantile esotropia cause, 220 nucleus lesions of, 440 palsies of, 101, 443–446 botulinum toxin treatment of, 353–355, 419–420 causes of, 352 congenital, 352 differentiated from infantile/ congenital esotropia, 219, 220

face turning associated with, 375 forced-generation test of, 169, 170 as lateral rectus muscle weakness cause, 226 lid ﬁssure widening associated with, 332, 353 Möbius syndrome-related, 364 as paralytic strabismus cause, 352–355 surgical treatment of, 353, 354–355 traumatic, 352–353 paresis of, Faden operation for, 400, 402 role in eye movements, 424–425 in supranuclear eye movements, 427, 428 Cranial nerve VII anomalies of, 469–470 in Möbius syndrome, 489–490 palsies of, 459–460 Cranial nerve XI, in Möbius syndrome, 489–490 Cranial nerve XII, in Möbius syndrome, 489–490 Craniofacial anomalies congenital exotropia associated with, 281 Möbius syndrome-related, 364 Craniofacial dysostosis, extraocular muscle aplasia-related, 365 Craniosynostosis, 369 ocular restriction associated with, 325, 327 Cross-ﬁxation, 123 Cianci’s syndrome-related, 228, 230, 231 Crowding phenomenon, 116 Cycloduction, 27, 62 Cyclomydril, 18, 521 Cyclopentolate, as cycloplegic agent, 18, 19, 172, 244, 521 Cyclopentolate test, for atropine penalization evaluation, 131 Cycloplegia, 17–20 Cycloplegic agents. See also speciﬁc cycloplegic agents side effects of, 521–522 Cyclotropia, 88 Cysts, of the iris, 253–254

index D Demerol, 4 Denver Developmental Scale, 2 Depth perception, monocular, 80–81 Dermoids, limbal, 17 Dextroversion, 67 Diabetes mellitus, as superior oblique paresis cause, 302 Diplopia acquired strabismus-related, 139, 174–177 antisuppression orthotopic therapyrelated, 273 convergence insufﬁciency-related, 277 crossed, 75, 177 in anomalous retinal correspondence, 183, 184 exotropia-associated, 203 head posturing associated with, 378 heterotropia-related, 84 horror fusionis-related, 188–189 intermittent exotropia-related, 267 Miller Fisher syndrome-related, 458 paradoxical, 182, 184 physiological, 73, 75–76 prism-induced, 95 torsional, retinal surgery-related, 348, 349 uncrossed, 75–76, 175, 177 esotropia-associated, 203 Diplopia tests, 190–204 Bagolini striated lens test, 179–180, 181, 184, 185, 190, 202–203 dissociating, 190, 193 Maddox rod test, 88, 165, 167, 190, 204, 301, 302, 307 red ﬁlter test, 190, 191, 192, 193–196 vertical prism red ﬁlter test, 196, 197, 198 Worth 4-dot test, 190, 196, 199–202 Dissociated horizontal deviation (DHV), 373 Dissociated vertical deviation (DVD), 370–373 asymmetrical, 370 bilateral, 370, 371, 373 deﬁnition of, 370 differentiated from inferior oblique muscle overaction, 310

537

infantile/congenital esotropiarelated, 225 inferior oblique overaction-related, 312 latent, 370 neurophysiological basis for, 372 primary, 370, 371 relationship with infantile esotropia surgery, 372–373 treatment of, 373 with superior oblique weakening procedure, 308 Divergence, 83 fusional, 95 normal amplitude of, 96 as position of rest, 26 Divergence insufﬁciency, 261 Divergence paresis, cranial nerve VI palsy-related, 352 “Dog on a leash” eye movement, 169, 171, 328 Doll’s head (oculocephalic) maneuver, 431 for double elevator palsy evaluation, 439 for infantile esotropia evaluation, 220, 221 for ocular motor cranial nerve palsy evaluation, 442 Donder’s law, 61–62 Dorsal midbrain syndrome, 435–438 Dorsolateral pontine nuclei (DLPN), 430 Dorsumduction, 27 Double elevator palsy, 316, 340–342, 439 Marcus Gunn jaw-winking-related, 468–469 Double vision. See Diplopia Duane’s cocontraction syndrome, 355–356 Duane’s syndrome, 355–362, 443 A- and V-pattern strabismus associated with, 284 adduction deﬁcits associated with, 310, 356–357, 358, 359, 360, 361, 362 bilateral, 359 bridle-effect theory of, 463–464 cause of, 355 cranial nerve IV anomalies associated with, 460–466 differentiated from infantile/ congenital esotropia, 219, 220

538

index

Duane’s syndrome (Continued) esotropia associated with, 219 face turning associated with, 375 horizontal rectus muscle cocontraction in, 32, 34 lateral rectus muscle weakness associated with, 226 limited adduction associated with, 325, 326 Marcus Gunn jaw-winking-related, 469 medial and lateral rectus muscle contraction in, 64 suppression associated with, 188 surgical treatment of for Duane’s syndrome type I, 361 for Duane’s syndrome type III, 361 for globe retraction, 361–362 indications for, 359–361 for upshoot and downshoot correction, 362 as synergistic divergence, 356, 357, 359 type I, 356, 357, 359 type II, 356, 357 type III, 356, 357, 359 X-pattern strabismus associated with, 286 unilateral, 359 Y-pattern strabismus associated with, 285 Ductions, 26–27, 63, 64, 65, 141, 142 forced. See Forced-duction testing limited, 323 Dysplasia, cortical and basal ganglia, 339 E Eccentric ﬁxation, 7 amblyopia-related, 117 differentiated from anomalous retinal correspondence, 184, 186 testing for, 117, 119 E game. See Illiterate E game Electromyography (EMG), in agonist and antagonist muscles, 63–64 Electro-oculography (EOG), 169 for cranial nerve VI palsy evaluation, 171 for horizontal and vertical eye movement measurement, 328

Empirical horopter, 71, 72, 73, 74–75 in stereoscopic vision, 74–75 Endophthalmitis, red reﬂex in, 15 Enophthalmos, 24 orbital ﬂoor fracture-related, 342 Epicanthal folds, in pseudo-strabismus, 229 Epstein-Barr virus infections, as Guillain-Barré syndrome risk factor, 457–458 Esophoria, 255 deﬁnition of, 86 divergence-based control of, 95 Esotropia, 217–265 accommodative, 243 bifocals for, 523–524 hypermetropic, 243–246 accommodative convergence (AC/A ratio) in, 99, 243, 246–247 acquired, 243 nonaccommodative, 254–255 acute comitant, 443–444 anomalous retinal correspondence associated with, 197 binocular vision in, 217 comparison with exotropia, 217 cortical suppression and, 107, 108 cover/uncover test for, 150–151 crossed diplopia associated with, 203 cyclic, 261 deﬁnition of, 86 Duane’s syndrome-related, 358, 359 surgical treatment of, 361 duration of, 217 fusional divergence correction of, 217 with high accommodative convergence (AC/A ratio), 243, 246–247 surgical treatment of, 251–252, 400, 402 Hirschberg test for, 146 incomitant, Faden operation for, 400, 402 infantile accommodative, 228, 245, 254 differentiated from infantile/ congenital esotropia, 219, 220–221 infantile/congenital, 217–243 amblyopia associated with, 223

index Esotropia (Continued) botulinum toxin treatment of, 242–243 characterization of, 221–222 Chavasse theory of, 219 Cianci’s syndrome-related, 228–231, 232 clinical assessment of, 226–227 clinical features of, 221 deﬁnition of, 217, 226 differential diagnosis of, 219, 220–221 differentiated from infantile accommodative esotropia, 219, 220–221 etiology of, 219–220 genetic factors in, 227–228 incidence of, 217–218 inferior oblique overactionrelated, 370 large-angle, 218, 221 latent nystagmus associated with, 225–226 motor abnormalities associated with, 225 onset of, 221 refractive errors associated with, 223–225 spontaneous resolution of, 222–223 strabismic amblyopia associated with, 113, 114 systemic associations of, 226 treatment of, 232–243, 372–373 types of, 228–232 Worth theory of, 219 large-angle, infantile esotropiarelated, 218, 221 Möbius syndrome-related, 364–365 neonatal, 105 with normal retinal correspondence, 193 nystagmus associated with, 255–260 face turning associated with, 255–256, 257 partially accommodative, 247–251 miotics treatment of, 252–254 surgical treatment of, 251–252 postoperative, 242 in intermittent exotropia patients, 276–277 prism-based neutralization of, 91, 92, 93

539

prism-induced, 94 refractive, 243 sensory, 261–262 differentiated from infantile/ congenital esotropia, 219 as uncrossed diplopia cause, 175 V-pattern, 450 chin depression associated with, 376 Ethmoid bone, endoscopic sinus surgery-related injury to, 365 Excitatory burst neurons (EBNs), 426–427, 429 Excycloduction (extorsion), 27 Excyclotropia (extorsion) deﬁnition of, 88 foveal location in, 89 Exophoria convergence-based control of, 95 deﬁnition of, 86 near, convergence insufﬁciencyrelated, 277 prism-induced, 96, 97 Exotropia, 86, 87, 266–283 accommodative convergence (AC/A ratio) in, 99, 269, 271, 272, 275 alternating, 87 A-pattern chin depression associated with, 376 treatment of, 287, 288 classiﬁcation of, 267 comparison with esotropia, 217 congenital, 279, 281 inferior oblique overactionrelated, 370 consecutive, 240 cover/uncover test for, 150–151 craniosynostosis-related, 369 crossed diplopia associated with, 177, 203 deﬁnition of, 86 Duane’s syndrome-related, 358, 359 surgical treatment of, 361–362 Hirschberg test for, 146 intermittent, 266–277 A- and V-patterns in, 275–276 accommodative convergence (AC/A ratio) in, 269, 271, 272, 275 basic, 269

540

index

Exotropia (Continued) bifoveal fusion in, 267 classiﬁcation of, 268–272 clinical features of, 266–267 measurement of deviation in, 272–273 natural history of, 267 nonsurgical treatment of, 273 normal, 266 postoperative care for, 276–277 proximal convergence in, 269 pseudodivergence excess in, 269, 270, 274–275 suppression associated with, 188 surgical treatment of, 273–275 tonic divergence excess in, 269, 270–272, 274–275 tonic fusional convergence in, 269 tropia phase increase in, 273–274 X-pattern, 276 Y-pattern, 285 large-angle, X-pattern, 286 left, cranial nerve III palsy-related, 362, 363 neonatal, 105 with normal retinal correspondence, 193 prism-induced, 92, 95 sensory, 280–281 Extorsion as excycloduction, 27 as excyclotropia, 88, 89 retinal, 167, 168 Extrafovel ﬁxation, amblyopia-related, 117 Extraocular muscles. See also Oblique muscles; Rectus muscles actions of, 27–28 agonists, 27, 63–64 anatomy of, 24, 25, 30–60 oblique muscles, 24, 25, 38–47 rectus muscles, 24, 25, 30–38 antagonists, 27, 63–64 aplasia of, 365, 368, 369 arcs of contact of, 27 congenital absence of, 480 disorders of, 479–480 fascial structures of pulleys (muscle sleeves), 49–51, 52, 55–56, 58 Tenon’s capsule, 52–58

ﬁbrosis of, 480 ﬁeld of action of, 28–29 histology of, 48–51 insertion of, 27 length of, 27 muscle ﬁber types of, 48 global layer (GL), 49, 50, 51 orbital layer (OL), 49, 50, 51, 52, 58 muscle-pulleys (muscle sleeves) of, 49–51, 52, 55–56, 58 abnormal location of, 325, 327 nerve ﬁber to muscle ﬁler innervation ratio to, 48 neuromuscular spindles of, 48–49 in ocular positioning, 24–26 origin of, 27 palsy of, deﬁnition of, 323 paresis of causes of, 323–324 deﬁnition of, 323 as incomitant strabismus cause, 100, 101–102 in smooth pursuit versus saccadic eye movements, 29–30 synergist, 64 tendon length of, 34 yoke muscles deﬁnition of, 67 Hering’s law of, 65–66, 67 Eye alignment, neonatal, 105 Eye examination, pediatric, 1–23 family history in, 2 medical history in, 1–2, 6 physical examination in, 1, 2–20 contrast sensitivity assessment in, 13–14 dilatation and cycloplegia in, 17–20 external examination in, 6 fundus examination in, 20 intraocular pressure measurement in, 16–17 keratometry in, 17 physician-patient rapport in, 2–4 pupillary examination in, 15–16 red reﬂex test in, 14–15 sedation use in, 4–5 slit-lamp examination in, 16 in uncooperative children, 4–5 visual acuity assessments in, 6–14

index Eye movements, 24–69. See also Ductions; Saccades; Smooth pursuit; Vergences development of, 105–106 limitation of, 325 ocular position, 24–26 range of, evaluation of, 424 reﬂex, evaluation of, 431 saccadic. See Saccades supranuclear, 423–440 disorders of, 432–440 physiology and clinical evaluation of, 424–431 vestibular, 424–425 F Face turning, 255–256, 257, 373–375 Brown’s syndrome-related, 315 congenital nystagmus-related, 376–378 cranial nerve VI palsy-related, 375 Duane’s syndrome-related, 358, 359, 375 treatment of, 359–360, 361 measurement of, 375 Facial anomalies congenital superior oblique palsyrelated, 301–302 cranial nerve VI palsy-related, 449–450, 451 Möbius syndrome-related, 490 myotonic dystrophy-related, 486 Facial palsy, Möbius syndrome-related, 364 Faden procedure, 333, 399–402 effect on accommodative convergence, 333 “Fallen eye,” 297–298 Far distance test, 273 Fat, orbital, 24, 25 entrapment of, 342, 343, 344. See also Fat adherence Fat adherence, 56–57, 411 deﬁnition of, 334 as ocular restriction cause, 325, 326 retinal surgery-related, 346–347 treatment of, 334–336 Fatigue, visual, intermittent exotropiarelated, 267 Fetal alcohol syndrome, 359 Fibrosis local anesthetics-related, 325, 326, 343, 345, 346 trochlear, 319

541

Fibrotic bands, congenital. See Congenital ﬁbrosis syndrome Fixation alternating, 120 infantile/congenital esotropiarelated, 224 Worth 4-dot test in, 199–200 normal development of, 7 Fixation preference testing, 8 for amblyopia, 199–122 for infantile/congenital esotropia, 226 for strabismus amblyopia, 10 Fixation reﬂex, 12 Fixation testing, 4, 6–8. See also Fixation preference testing for amblyopia, 119–122 in eccentric ﬁxation, 117, 119, 120 with monocular ﬁxation testing, 119 with Visuscope, 119 binocular, 6, 7–8 monocular, 6–7, 8 Forced-choice preferential looking (FPL) test, 9–10 Forced-duction testing, 168, 169, 170, 329–331 in Brown’s syndrome, 315 Forced-generation testing, 331 Forced lid closure test, 431 Four base-out test, 212, 214–216 Fovea angle kappa of, 145–149 maturation of, 7 Foveal ectopia, 348 Fresnel Press-On prisms, 528 Fundus, examination of, 20, 172 Fusion diplopia test-related disruption of, 190 with Maddox rod test, 193, 204 with red ﬁlter test, 193 with Worth 4-dot test, 193, 196, 200–201 four base-out test for, 212, 214–216 latent strabismus-related disruption of, 139 Fusional tests, 3 G Gaucher’s disease, 432, 433 saccade initiation failure associated with, 432, 433, 434

542

index

Gaze cardinal positions of, 142 measurement of, 155 positions of, 28 Glasses. See Spectacles Glaucoma explant surgery, as strabismus cause, 349–351 Globe retraction Duane’s syndrome-related, 361–362 Möbius syndrome-related, 364 Goldenhar’s syndrome, 359 Goldmann perimetry, 12 Goniometers, orthopedic, 374–375 Gradenigo’s syndrome, as cranial nerve VI palsy cause, 352 Graves’ disease/ophthalmology deﬁnition of, 336 inferior rectus muscle recession in, 333–334 management of, 336–338 as ocular restriction cause, 326 Guillain-Barré syndrome bulbar variant of, 457 cranial nerve palsy associated with, 457–458 differentiated from botulism, 479 infections as risk factor for, 457–458 relationship with Miller Fisher syndrome, 458–459 H Haemophilus inﬂuenzae infections, 452 Hang-back recession, 393–394, 396 Haploscopic devices, 77–78 Haploscopic tests, 204–212 amblyoscope-based, 204, 205–209 Lancaster Red/Green test, 164–165, 166–267, 204–205 Harada-Ito procedure, 42, 304, 349, 412–413, 451 bilateral, 305 Headaches, migraine. See Migraine headaches Head posturing, abnormal, 373–379. See also Face turning; Head tilt; Torticollis as binocular fusion indicator, 139 incomitant strabismus-related, 375–376 nystagmus-related, 379 surgical treatment of, 376–378 Head-thrusting behavior, in saccade initiation failure (oculomotor apraxia), 433–434

Head tilt congenital superior oblique paresisrelated, 301, 302 cranial nerve IV palsy-related, 449, 450, 451 nystagmus-related, 378 traumatic superior oblique paresisrelated, 300 Head tilt test for differentiation of primary from secondary inferior oblique overaction, 310–311 in inferior oblique paresis, 305 in superior oblique overaction, 305 Head trauma as cranial nerve III palsy cause, 363 as cranial nerve IV palsy cause, 443–444, 451–452 as cranial nerve VI palsy cause, 352 as esotropia cause, 443–444 as inferior oblique palsy cause, 304 as superior oblique paresis cause, 297, 299–300 Heavy eye syndrome, 351 Hering’s law of equal innervation, 144, 474 esotropia neutralization and, 93 hypertropia and, 87 incomitant deviations and, 159 oblique overaction and, 290 primary deviation and, 101 prism-induced vergence and, 95 right amblyopia and, 123 superior oblique paresis and, 295 true hypertropia and, 370 vergence eye movements and, 82, 95 yolk muscles and, 65–66, 298–299 Herpes zoster ophthalmicus, 302 Heterophoria, deﬁnition of, 84 Heterophoria method, of accommodative convergence (AC/A ratio) measurement, 161–162 Heterotropia, deﬁnition of, 84 Hirschberg reﬂex, 126 Hirschberg test, 144–145, 146, 147, 152 corneal light reﬂex in, 524 photographic techniques in, 524 Homatropine, as cycloplegic agent, 18, 19 Horizontal rectus muscles. See also Lateral rectus muscle; Medial rectus muscle action of, 27

index Horizontal rectus muscles (Continued) anatomy of, 32–35 Duane’s syndrome-related cocontraction of, 24 transposition of, 403, 407 as A- or V-pattern strabismus treatment, 287–288, 289 as superior oblique muscle overaction treatment, 308 Horror fusionis, 188–190 HOTV letters, 11, 14, 118 Hummelsheim procedure, 404, 405, 406, 419 for cranial nerve VI palsy, 353, 354, 355 for medial rectus hypoplasia, 365, 369 for medial rectus muscle injury, 365 modiﬁcations of, 354, 406 for monocular elevation deﬁcit syndrome, 342 Hydrocephalus dorsal midbrain syndrome associated with, 436, 438 internuclear ophthalmoplegia associated with, 441 setting sun sign associated with, 437 Hypermetropia amblyopia-related, 115–116 bilateral, spectacles use in, 127, 128 infantile/congenital esotropiarelated, 223–224, 225 with overconvergence, as infantile esotropia cause, 219 Hyperopia high, lens-based correction of, 522–523 infantile/congenital esotropiarelated, 224–225 in neonates, 522 Hypertropia, 87 bilateral superior oblique paresisrelated, 296, 297 cover/uncover test for, 150–151 dissociated vertical deviationrelated, 370 Hirschberg test for, 146 left, 87–88 diplopic image in, 177 oblique muscle palsy-related, 292–294 prism-induced, 92

543

rectus muscle palsy-related, 292–294 right, 87–88 superior oblique paresis-related, 302–303 true, 370 vertical vergence-based control of, 95 Hypoaccommodation, cranial nerve III palsy-related, 362 Hypotonia, in saccade initiation failure, 434 Hypotropia, 87 cranial nerve III palsy-related, 362, 363 I I-ARM acronym, for pediatric screening examination, 125, 126 Illiterate E game, 11, 14, 118, 141 Image jump, 79, 90, 91 Immunizations as cranial nerve III palsy cause, 452 as cranial nerve VI palsy cause, 352 Immunosuppressive therapy, for myasthenia gravis, 476–477 Incycloduction, 27 Incyclotropia, 88 foveal location in, 89 Induced convergence retraction, 435–438 Induced tropia test, 122–125 Infarction, as cranial nerve III palsy cause, 452 Infections, as Guillain-Barré syndrome cause, 457–458 Inferior oblique muscle actions of, 27, 42, 45 anatomic insertion of, 27 anatomic relationship with inferior rectus muscle, 36–37, 38–39 lateral rectus muscle, 34–35 vertical rectus muscle, 40, 41 anatomy of, 40, 41, 42, 45–47 arc of contact of, 27 ﬁeld of action of, 28 length of, 27 origin of, 27 palsies of adduction deﬁcits associated with, 306, 316 eye movement limitations in, 29

544

index

Inferior oblique muscle (Continued) pareses of isolated, 304–305 unilateral, 305–306 pseudo-overaction, 310 tendon length of, 34 weakness of, 439 yoke muscle function of, 66 Inferior oblique muscle overaction, 308–312 with A- or V-pattern strabismus, 288 bilateral asymmetrical, 311 craniosynostosis-related, 369 differentiated from dissociated vertical deviation, 370 dissociated vertical deviationrelated, 373 infantile/congenital esotropiarelated, 225, 370 intermittent exotropia-related, 275 mimickers of, 310–311 primary, 308–310 differentiated from secondary inferior oblique overaction, 309–310 V-pattern, 309, 311 Y-pattern, 309–310, 311 superior oblique paresis versus, 299 treatment of. See Inferior oblique muscle weakening procedures unilateral asymmetrical, 311 Inferior oblique muscle recession, 311, 391, 407, 408 Inferior oblique muscle weakening procedures, 311–312, 407–411 anteriorization (anterior transposition), 45–47, 311–312, 407–410 as dissociated vertical deviation treatment, 373 graded anteriorization technique of, 47 J-deformity associated with, 46–47, 312, 409, 410 as ocular restriction cause, 46–47, 327 extirpation-denervation, 407 graded recession-anteriorization, 410–411 myotomy, 407 recession, 311, 391, 407, 408 Inferior rectus muscle actions of, 27, 36

anatomic insertion of, 27 anatomic relationship with inferior oblique muscle, 36–37, 38–39 anatomy of, 30, 36–38 fascial connections, 36–37, 38–39 aplasia of, 365, 368 arc of contact of, 27 hypoplasia of, 365, 368 length of, 27 lost, 37 origin of, 27 paresis of, left, 290 tight, double elevator palsy-related, 340, 341 transposition of, 406–407 Inferior rectus muscle recession lid changes associated with, 37 in thyroid strabismus, 337 Inferior rectus muscle resection, lid changes associated with, 37 Inﬂammation, as cranial nerve VI palsy cause, 443, 446 Infraduction, 27 Infrared eye trackers, 328 Infraversion, 67 Ing, Malcolm, 235 Inhibitional palsy of the contralateral antagonist, 298–299 Inhibitory burst neurons (IBNs), 426–427, 429 Intermuscular septum, 53, 54 Internuclear ophthalmoplegia, 440–441 Interpupillary distance effect on stereoacuity, 78 relationship with convergence, 161 Interstitial nucleus of Cajal, lesions of, 372 Intorsion, retinal, 167 Intrafacial synkinesis, 469 Intraocular pressure (IOP) elevated, 16 ocular restriction-related, 331 measurement of, 16–17 propofol-related decrease in, 4, 5, 17 Iris, vascular supply to, 58–59 Ischemia, of the anterior segment, 59–60, 354, 406 J J-deformity, 46–47, 312, 409, 410 Jensen procedure, 404, 405 Joubert syndrome, 339

index K Kearns-Sayre syndrome, 481–485 chronic progressive external ophthalmoplegia associated with, 482–484 cranial nerve palsy associated with, 456 Keratometry, 17 Kestenbaum-Anderson-Parks procedure, 376–378 Klippel-Feil syndrome, 359 Koerber-Salus-Elschnig syndrome, 435 Krimsky light reﬂex test, 149, 150, 227, 524, 527 L Lancaster Red/Green test, 164–165, 166–167, 204–205 Lateral geniculate nucleus (LGN), in amblyopia, 110, 111, 113–114, 190 Lateral rectus muscle actions of, 27, 32 anatomic insertion of, 27 vertical displacement of, 32 anatomic relationship with inferior oblique muscle, 34–35 anatomy of, 30, 34–35 in anterior segment blood circulation, 59 arc of contact of, 27, 34 congenital aberrant innervation of, 285 in cranial nerve VI palsy, 354 Duane’s syndrome-related cocontraction of, 355–356, 357 infraplacement of, 275–276 with intermuscular septum and check ligaments, 54 “leash effect” of, 286 length of, 27 lost, 34–35 myopic strabismus ﬁxus-related slippage of, 351 origin of, 27 recession of as A-pattern strabismus treatment, 287, 288 bilateral, as intermittent exotropia treatment, 274–275 ipsilateral, as dissociated horizontal deviation treatment, 373 tendon length of, 34 yoke muscle function of, 65, 66

545

LEA ﬁgures, 11, 118 Lens gradient method, of accommodative convergence (AC/A ratio) measurement, 161–162, 163–164 Lens implants, ultraviolet protection for, 524 Levator palpebrae, anatomic relationship with superior rectus muscle, 36 Levodopa/carbidopa, as amblyopia treatment, 132 Levoversion, 67 Lid ﬁssure narrowing of, 24 Duane’s syndrome-related, 356–357 inferior rectus muscle recession-related, 37 ocular restriction-related, 331 widening of, 24 inferior rectus muscle recession-related, 37 rectus muscle paresis-related, 331–332 Lidocaine, myotoxic effects of, 343 Lid retraction, in dorsal midbrain syndrome, 436 Lid speculum, 4 wire, 3 Light occlusion, bilateral, as amblyopia treatment, 131–132 Light reﬂex tests, 144–150 angle kappa, 145–149 Brückner test, 15, 126, 127, 149–150, 249, 358 Hirschberg test, 144–145, 146, 147, 152 Krimsky test, 149, 150, 227, 524, 527 Line of sight, angle kappa of, 145–146 Listing’s law, 61–62 Listing’s plane, 61 Local anesthetics, myotoxic effects of, 343, 345–346 Lockwood’s ligament, 37, 38, 39, 45 Long-lead burst neurons (LLBNs), role in saccadic eye movements, 429 M Macular degeneration, color vision assessment in, 12 Maculopathy, ultraviolet protection in, 524

546

index

Maddox rod test, 88, 165, 167, 190, 204 in congenital superior oblique palsy, 301, 302 double, 165, 167 single, 165 in superior oblique overaction, 307 Marcaine, myotoxic effects of, 343 Marcus Gunn jaw-winking phenomenon, 341, 468–469 Duane’s syndrome-related, 359 Marin-Amat syndrome, 470 M cells, 373 Measles, as Guillain-Barré syndrome cause, 457–458 Medial longitudinal fasciculus lesions, 440–441 Medial rectus muscle actions of, 27, 32, 33 anatomic insertion of, 27 vertical displacement of, 32 anatomy of, 30, 34 arc of contact of, 27 in Cianci’s syndrome, 229, 231 Duane’s syndrome-related cocontraction of, 355–356 endoscopic sinus surgery-related injury to, 365, 366–367 in Faden procedure, 400 length of, 27 lost, 56 origin of, 27 tendon length of, 34 tight, Möbius syndrome-related, 364–365 yoke muscle function of, 65, 66 Medial rectus muscle recession, 390–391 bilateral, 304 asymmetrical, 333 as congenital esotropia treatment, 232–242 as partially accommodative esotropia treatment, 247–252 right, 332–333 as Möbius syndrome treatment, 365 Medial rectus muscle shortening, right, 396–397 Medulloblastomas, as cranial nerve VI palsy cause, 443 Megacolon, Hirschsprung, 469 Meningitis cranial nerve VI palsy associated with, 352, 443

internuclear ophthalmoplegia associated with, 441 Mesencephalic-diencephalic junction lesions, 435 Mesencephalic reticular formation, 430 Micrognathia, Möbius syndromerelated, 364 Microtropias, binocular ﬁxation preference testing in, 8 Migraine headaches as esotropia cause, 443–444 ophthalmoplegic, 455–456 Miller Fisher syndrome, 441, 457, 458–459 relapsing, 459 Miotics as accommodative esotropia treatment, 252–254 side effects of, 253–254 Misoprostol, as Möbius syndrome risk factor, 364 Möbius syndrome, 364–365 differentiated from infantile/ congenital esotropia, 219, 220 Monocular depth perception, 80–81 Monocular elevation deﬁciency, 439 Monocular ﬁxation syndrome. See Monoﬁxation syndrome (peripheral fusion) Monocular vision, development of, 103 Monoﬁxation syndrome (peripheral fusion), 89, 172–182 amblyoscope testing in, 206 anisometropic amblyopia-related, 114 Bagolini striated lenses test in, 203 cover test in, 152, 154 as ocular restriction cause, 326 primary, 182 Worth 4-dot test in, 200–201 Motility disorders, ocular, 423–519 disorders at the neuromuscular junction, 470–479 disorders of nerve and muscle, 481 Kearns-Sayre syndrome, 481–485 Möbius syndrome, 489–491 myotonic dystrophy, 485–489 disorders of the central and peripheral nervous systems, 423–470 anomalies of innervation, 460–467

index Motility disorders, ocular (Continued) internuclear ophthalmoplegia, 440–441 ocular motor cranial nerve palsies, 442–470 supranuclear disorders, 432–440 disorders of the extraocular muscles, 479–480 Möbius syndrome-related, 364 Motion parallax, 80–81 Motor abnormalities, esotropia associated with, 225 Motor examination, ocular, 138–173 family history in, 139 goals of, 138 medical history in, 138–139 physical examination in, 139–172 accommodative convergence measurement in, 161–164 amblyopia assessment/visual acuity assessment in, 140–141 binocular sensory testing in, 139 clinical distance-near relationship in, 164 cycloplegic refraction in, 172 ductions and versions in, 140, 141–143 fundus examination in, 172 inspection of patients in, 140 Lancaster Red/Green test in, 164–165, 166–167 ocular deviation measurements in, 140, 143–160 restriction and paresis tests in, 168–172 sensory tests in, 141 torsion assessment in, 164–168 Motor fusion, 70, 81–83 in binocular vision, 70, 81–83 deﬁnition of, 81–82 fusional vergence movements in, 82 phoria-related decrease in, 84, 85 torsional, 88–89 MTI PhotoScreener, 10, 15 Multiple sclerosis contrast sensitivity in, 14 internuclear ophthalmoplegia associated with, 441 superior oblique paresis associated with, 302

547

Mumps, as Guillain-Barré syndrome cause, 457–458 Muscle pull, mechanical disadvantage of, 324 Muscle-pulleys (muscle sleeves), of extraocular muscles, 49–51, 52, 55–56, 58 abnormal location of, 325, 327 Muscle recession procedures, 388–396 adjustable suture technique in, 394–396 hang-back technique in, 393–394, 396 as incomitant strabismus treatment, 332 inferior oblique, 311, 391, 407, 408 inferior rectus, 37, 337 lateral rectus, 274–275, 287, 288, 373 recession-resection (“R and R”) procedure, 399 rectus, 388–391 Starling’s length-tension curve in, 388, 389, 390 superior rectus, 36, 373 Muscle shortening procedures, 396–399 plications, 396, 398–399 resections, 332, 396, 397 tucks, 396, 397–398 Muscle transposition procedures, 402–407 anteriorization (anterior transposition), inferior oblique, 45–47, 311–312, 407–410 as dissociated vertical deviation treatment, 373 graded anteriorization technique of, 47 J-deformity associated with, 46–47, 312, 409, 410 as ocular restriction cause, 46–47, 327 complications of, 406 of horizontal rectus muscle, 403, 407 as A- or V-pattern strabismus treatment, 287–288, 289, 403 as superior oblique muscle overaction treatment, 308 for rectus muscle palsy, 404–406 complications of, 406 Hummelsheim procedure, 405, 406

548

index

Muscle transposition procedures (Continued) Jensen procedure, 404, 405 Knapp procedure, 404, 405 for small vertical deviations, 403 split-tendon Hummelsheim procedure, 353, 354, 355, 365, 369, 404, 405, 406, 419 Jensen procedure, 404, 405 for torsion, 406–407 of vertical rectus muscles, 345, 406, 407 Muscular dystrophy, facio-scapulohumeral, 490 Myasthenia gravis autoimmune (acquired), 472–477 congenital, differentiated from infantile/congenital esotropia, 219, 220 as cranial nerve VI palsy cause, 352 differentiated from internuclear ophthalmoplegia, 441 Mydriasis atropine-related, 521 comparison with cycloplegia, 172 cyclopentolate-related, 521 Mydriatic drops, as discomfort cause, 4 Myectomy, of inferior oblique muscle, 311 Myopathies congenital centronuclear (myotubular), 490 dysthyroid, 480 proximal myotonic, 485, 486–487, 488 Myopia alternating, infantile/congenital esotropia-related, 225 binocular visual acuity in, 522 high, 351 acquired strabismus ﬁxusrelated, 351–352 lens-based correction of, 522 in neonates, 522 Myotonic dystrophy, 485–489 N Near ﬁxation targets, 3 Near point convergence exercises, 278–279 Near point of convergence (NPC), in convergence insufﬁciency, 278

Near reﬂex, 99 spasm of, 439–440 Near targets, accommodative, 3 Near triad, 430 Neisseria meningitidis infections, 452 Neosynephrine, 172 Nephronophthisis, 435 Neural integrator, 429 deﬁnition of, 430 evaluation of, 431 Neuroblastomas, 469 Neurological diseases as comitant strabismus cause, 100 differentiated from infantile/ congenital esotropia, 219 Neurological evaluation, of acquired strabismus patients, 139 Neuromuscular blocking agents, as myasthenia gravis cause, 472 Neuromuscular junction disorders, 470–479 autoimmune (acquired) myasthenia gravis, 472–477 botulism, 478–479 congenital myasthenic syndrome, 471–472 familial infantile myasthenia gravis, 470–471 transient neonatal myasthenia, 470 Neuromyopathies, 456–457 Neurons binocular cortical, 104–105 monocular cortical, 104 Neuropathies generalized, 457 progressive optic, 12 Niemann-Pick disease, 434 Nucleus reticularis tegmenti pontis (NRTP), 430 Nystagmus Cianci’s syndrome-related, 228–229, 231 congenital, esotropia associated with, 257 258, 259 gaze-evoked, 431, 474 head posturing associated with, 374, 375, 378–379, 379 treatment of, 376–378 head tilt associated with, 378 latent with cyclovertical movement, 370, 372 esotropia-related, 255–256, 257

index Nystagmus (Continued) infantile/congenital esotropiarelated, 225–226 manifest, 257, 258, 378–379 visual acuity testing in, 123, 125 optokinetic (OKN), 8–9, 65. See also Optokinetic nystagmus (OKN) drum; Optokinetic nystagmus (OKN) testing evaluation of, 429 normal development of, 7 in saccade initiation failure, 432–433 rebound, 431 seesaw, 372 sensory, 115 surgical treatment of, 378 vestibular, evaluation of, 429 Nystagmus compensation (blockage) syndrome, 259–260 cyclovertical, 372 O Oblique muscle(s). See also Inferior oblique muscle; Superior oblique muscle actions of, 27–28, 39–40 anatomic relationship with rectus muscles, 24 anatomy of, 24, 25, 39–47 dysfunction of, 289–319 clinical evaluation of, 289–290 primary overaction of, differentiated from paresis Bielschowsky head tilt test for, 290–291, 294 three-step test for, 291, 292–294 retinal surgery-related displacement of, 347–348 Oblique muscle recessions, 391 Occlusion test for exotropia measurement, 272 in combination with far distance test, 273 for intermittent exotropia measurement, 274–275 for pseudodivergence excess measurement, 270–271 Occlusion therapy, 3 for amblyopia, 130, 131–132 effect on contrast sensitivity, 14 part-time, for exotropia, 273

549

Ocular deviations, measurement of, 140, 143–160 accommodation targets in, 144 accommodative convergence (AC/A ratio), 161–164 cover tests for, 4, 150–159, 528–529 alternate cover test, 152–153, 154, 157 for cardinal positions of gaze measurement, 155 cover/uncover test, 149, 150–152, 154 interpretation of, 152, 154 prism alternate cover test, 154 simultaneous prism cover test, 155–156 variable measurements in, 154–155 incomitant deviations measurement, 159, 160 light reﬂex tests, 144–150 angle kappa, 145–149 Brückner reﬂex test, 149–150 Hirschberg test, 144–145, 146, 147, 152 Krimsky test, 149, 150, 227, 524, 527 methods of, 144 prism-based methods, 143–144 with Snellen letters, 144 Ocular muscle contraction moment arm in, 388, 389 rotational force in, 388, 389 Ocular tilt reaction, 450 Oculocephalic maneuver. See Doll’s head (oculocephalic) maneuver Oculomotor nerve. See Cranial nerve III Oculomotor reﬂexes, 65 Oculomotor synkinesis, 453–454, 467 cranial nerve III palsy-related, 362–363 Omnipause neurons, role in saccadic eye movements, 429 One and one-half syndrome, 474 Ophthalmoplegia chronic progressive external, 482–484 generalized neuropathies-related, 457 internuclear, 440–441 Optical pearls and pitfalls, 520–529 Optic nerve, hypoplasia of, 370 Optic nerve, myelination of, 7

550

index

Optokinetic nystagmus (OKN) drum, 7, 9, 30, 65, 169, 328–329 Optokinetic nystagmus (OKN) testing in congenital ﬁbrosis syndrome, 232 for saccadic eye movement diagnosis, 30, 226–227, 328–329 for smooth pursuit asymmetry diagnosis, 106 Optotype testing, 11–12, 141 Oral clefts, Möbius syndrome-related, 364 Orbit craniosynostosis-related extorsion of, 369 fractures of, as ocular restriction cause, 326 Orbital decompression, as Graves’ ophthalmology treatment, 336–337 Orbital ﬂoor fractures, as restrictive strabismus cause, 342–345 Orbital mass, as ocular restriction cause, 325, 326 Orthophoria, 84–85 Orthostatic reﬂex, 65 Orthotropia, 84 Otoliths, 425 P Palpebral ﬁssure, Duane’s syndromerelated narrowing of, 359–360 Palsy. See also Strabismus, paralytic; speciﬁc palsies deﬁnition of, 323 Panum’s fusional area binasal retinal stimulation within, 76, 77–78 bitemporal retinal stimulation within, 76–77 in physiological diplopia, 75, 76 Papoose boards, 3, 4 Paramedian pontine reticular formation, 427, 428, 429, 437 Paresis. See also Strabismus, paralytic; speciﬁc pareses deﬁnition of, 323 diagnostic tests for, 168, 169, 170, 171–172 Parkinson’s disease, as accommodative insufﬁciency cause, 280 Parks, Marshall, 334, 416 Parks-Bielschowsky three-step test, 449 Patching. See Occlusion therapy Patch test. See Occlusion test

Penalization, as amblyopia treatment, 130–131 atropine, 130–131, 523 ultraviolet protection during, 524 optical, 130 Pencil pushups, 279 D-Penicillamine, as myasthenia gravis cause, 472–473 Perkins tonometer, 16–17 Pertussis, as Guillain-Barré syndrome cause, 457–458 Peters’ anomaly, bilateral, 115 Pfeiffer syndrome, 369 Phenergan, 4, 5 Phenothiazines, as myasthenia gravis cause, 472 Phenylephrine, as cycloplegic agent, 18, 19 Phorias cover/uncover test for, 151 deﬁnition of, 84 differentiated from tropias, 204 intermittent, 85 spontaneous manifestation of, 85 Phoria-tropia syndrome, 179 Phospholine iodide, 252–253 side effects of, 253–254 Photophobia, intermittent exotropiarelated, 267 Photoscreening, 10, 15 Physical restraint, of uncooperative patients, 3, 4 Physostigmine, 18 side effects of, 521 Pinealomas, as dorsal midbrain syndrome cause, 436 Placido’s disc, 17 Plagiocephaly, congenital superior oblique palsy-related, 301–302 Plasticity, prolonged visual, 190 Pleoptics, as amblyopia-related eccentric ﬁxation treatment, 132 Plications, 396, 398–399 Pneumotonometers, 17 Podnar, Gregg, 118 Podnar, Paul, 118 Portal Stimuli System (Haag-Streit), 118 Position, ocular, 24–25 Position of rest, 26 Prader-Willi syndrome, 339 Premature infants retinopathy in, 147, 148 tonic downgaze in, 439

index Presbyopia, 280 Pretectal sign, 435 Prism adaptation, 252, 255 Prism alternate cover test, 154 Prism convergence exercises, 278 Prism diopters (PD), 90–91, 524 conversion to degrees, 525 use in fusional vergence amplitude measurement, 95–96, 98 Prisms, ophthalmic for ocular deviations measurement, 143–144 for strabismus measurement and correction, 524–529 additivity error with, 526–527 base-down, 95 base-in, 92, 94, 95–96 base-out, 91–92, 95, 96, 97, 98 base-up, 92, 95 in exotropia, 272 for face turning measurement, 375 in four base-out test, 212, 214–216 Fresnel Press-On, 528 image jump effect of, 79, 90, 91 in incomitant strabismus, 528–529 in Krimsky test, 149, 150 loose, 3 at near ﬁxation, 527 nomograms for, 527, 528 oblique, 527–528 positioning of, 525–526 in simultaneous prism cover test, 155–157 “stacking” of, 526–527 strabismus-inducing, 92, 94–95, 96 strabismus-neutralizing, 91–92, 93, 528–529 through glasses, 527 Propofol, 4, 5 Proprioceptive eye position control, 99 Proptosis, 24 Graves’ disease-related, 336–337 Prostigmin, 475 Proximal myotonic myopathy, 485, 486–487, 488 Pseudo-Brown’s syndrome, 327, 349 Pseudo-esotropia, 220, 228 differentiated from infantile/ congenital esotropia, 219, 220

551

Pseudo-fovea in anomalous retinal correspondence, 182, 183, 184, 185, 186, 202–203, 207–209 in vertical prism red ﬁlter test, 196, 197, 198 Pseudointernuclear ophthalmoplegia, 458 Pseudo-strabismus, 229 Pseudotorsion, 62 Ptosis chin elevation associated with, 374, 378–379 cranial nerve III palsy-related, 362–363, 364 treatment of, 363, 364 myasthenia gravis-related, 473, 474, 475 myotonic dystrophy-related, 488–489 Pulled-in-two syndrome (PITS), 347 Pulleys. See Muscle-pulleys Pupillary dilation, 17–18, 19 cranial nerve III palsy-related, 362 Pupillary light reactor, normal development of, 7 Pupils Adie’s, as accommodative insufﬁciency cause, 280 distance between relationship with convergence, 161 examination of, 4, 15–16 pupillary distance between effect on stereoacuity, 78 size of, age-related variations in, 15 Purkinje image, ﬁrst, 144–145 Purkinje-Sanson image, ﬁrst, 524 Q Quinine, as myasthenia gravis cause, 472 “Quiver movements,” 474 R Ragged-red ﬁbers, 482, 487 Random dot stereoacuity test, 79–80 Reading aids for accommodative insufﬁciency patients, 280 for anisometropic myopic amblyopia patients, 523 Recession procedures. See Muscle recession procedures

552

index

Recession-resection (“R and R”) procedure, 399 Rectus muscle(s). See also Lateral rectus muscle; Medial rectus muscle anatomic relationship with oblique muscles, 24 anatomy of, 24, 25, 30–38 forced-duction testing of, 329–331 innervation of, 31 insertion of, 30–31 length of, 31 lost, 55–56, 418–419 in ocular positioning, 24, 25 palsies of differentiated from ocular restriction, 325 forced-duction testing in, 329–331 forced-generation testing in, 331 preoperative diagnosis of, 330–331 pseudoinferior, 342, 343 transposition surgery for, 404–406 paresis of, as saccadic eye movement loss cause, 327 in saccadic eye movements, 30, 327 slipped, 55–56, 418–419 as ineffective muscle pull cause, 324 retinal surgery-related, 347 surgical procedures on, 388–391 Faden procedure, 399–402 plication, 398–399 recession, 24, 388–392 tightening procedures, as lid ﬁssure narrowing cause, 24 Red ﬁlter test, 190, 191, 192, 193–196 Red reﬂex test, 4, 14–15, 125, 126–129 Refraction, 19, 20 cycloplegic, 172, 521 effect of eye pigment on, 172 in hypermetropic accommodative esotropia, 244 for infantile/congenital esotropia evaluation, 227 Refractive errors esotropia associated with, 223–225 as head posturing cause, 379 high, lens-based correction of, 523 as strabismus cause, 85

strabismus-related, lens-based correction of, 523 Resection procedures. See Muscle resection procedures Restriction, ocular causes of, 325–327 deﬁnition of, 325 differentiated from paresis, 327–332 test for identiﬁcation of, 168–171 Retinal correspondence anomalous (ARC), 117, 182–188 afterimage test of, 209, 210–211, 212 amblyoscope testing in, 207–209 angle of anomaly in, 186, 207 Bagolini striated lenses test in, 202–203 deﬁnition of, 182 differentiated from eccentric ﬁxation, 184, 186 differentiated from normal retinal correspondence, 193, 196, 197, 198 harmonious, 186, 207–208 paradoxical diplopia associated with, 183, 184, 187 pseudo-fovea in, 182, 183, 184, 185, 186, 202–203, 207–209 red ﬁlter test in, 192, 193 unharmonious, 186, 187, 208–209 normal (NRC) afterimage test of, 209, 210–211 amblyoscope testing in, 205, 206 Bagolini striated lenses test in, 202, 203 deﬁnition of, 182 differentiated from anomalous retinal correspondence, 193, 196, 197, 198 red ﬁlter test in, 191, 193 Retinal image, blurred bilateral, 115–116 Retinal rivalry, 81, 82 Retinal surgery, as strabismus cause, 346–349 Retinopathy of prematurity, positive kappa angle in, 147, 148 Retinoscopy dry, 520 dynamic, 520–521 Retinoscopy lens, loose, 3

index Retrobulbar anesthetic blocks, 42 Rheumatoid arthritis, as Brown’s syndrome cause, 315, 316 Richmond pseudoisochromatic plates, 13 Rivalry, retinal, 81, 82 Rotation, ocular limitation of, 325 physiology of, 61–67 cycloduction, 62 Donder’s law of, 61–62 Listing’s law of, 61–62 pseudotorsion, 62 Sherrington’s law of reciprocal innervation, 63–64 synergist muscles, 64 Rubinstein-Taybi syndrome, 469 S Saccade initiation failure, 432–435 acquired, 432, 433 congenital, 432, 433 Saccades, 29–30 abnormalities of, 429 amplitude of, 29 command-generated, 425 deﬁnition of, 29 evaluation of, 328–329, 425 preoperative, 328 involuntary, 425 memory-guided, 425 in neonates, 7, 105 normal development of, 7 optokinetic nystagmus-based evaluation of, 30, 226–227 physiology of, 426–429 reﬂex, 425 elicitation of, 429 smooth pursuit eye movements versus, 29–30 spontaneous, 425 upward, brainstem pathways in, 437 voluntary, 425 Saccadic omission, 30 Saccadic velocity measurement, 169, 171 for differentiated of restriction from paresis, 327–329 of lateral rectus muscle function, 354 Schiotz tonometer, 16 Scleral buckling procedure, as strabismus cause, 346, 347

553

Scotomas large, Worth 4-dot test in, 200 suppression, 107 Bagolini striated lenses test in, 203 facultative, 180 large-scale strabismus-related, 188, 189 monoﬁxation syndromerelated, 179–182 red ﬁlter test in, 194 vectograph examination of, 214 Worth 4-dot test in, 202 Sedation contraindication in adjustment suture technique, 396 during intraocular pressure measurement, 17 during keratometry, 17 during slit-lamp examination, 16 of uncooperative patients, 4 Sedatives, exotropia-inducing effect of, 266 Semicircular canals, 424–425 Sensory adaptations, to strabismus, 85, 174–216 deﬁnition of, 174 sensory tests for, 141, 190–216 afterimage test, 209–212 diplopia tests, 190–204 four base-out test, 212, 214–216 haploscopic tests, 204–212 vectographic tests, 212, 213–214 visually immature, 174, 178–190, 178–216 anomalous retinal correspondence, 182–188 horror fusionis, 188–190 large retinal suppression, 188, 189 monoﬁxation syndrome (peripheral fusion), 172–182 prolonged visual plasticity, 190 visually mature, 174–178 confusion, 177–178 diplopia, 174–177 Sensory fusion, in binocular vision, 70–83 binocular cortical cells in, 70, 71 corresponding retinal points in, 70–71

554

index

Sensory fusion, in binocular vision (Continued) deﬁnition of, 70 disparate images in, 72 empirical horopter in, 71, 72, 73, 74–75 noncorresponding retinal points in, 72, 73 Panum’s fusional area in, 72, 73, 74 stereoacuity testing in, 76–80 stereoscopic vision in, 72, 74–75 Vieth-Müller circle in, 71, 72 Sensory tests, 141, 190–216 afterimage test, 209–212 diplopia tests, 190–204 four base-out test, 212, 214–216 haploscopic tests, 204–212 vectographic tests, 212, 213–214 Setting sun sign, 437 Sherrington’s law of reciprocal innervation, 63–64, 171, 331–332, 352, 391 Silicone frontalis sling procedure, 364 Simultaneous prism cover test, 155–157 Sinus disease, cavernous, as cranial nerve VI palsy cause, 352 Sinusitis, as Brown’s syndrome cause, 315, 316 Sinus surgery, as medial rectus muscle injury cause, 365, 366–367 Skiascopy rack, 20 Slip lamps, portable, 3 Slipped muscles, in strabismus surgery, 53, 55–56 Slit lamp examination, 16 Smooth pursuit, 425, 429–430 accurate, as visual development milestone, 106 in neonates, 7, 105–106 neural pathways for, 429–430 purpose of, 429 saccadic eye movements versus, 29–30 Smooth pursuit asymmetry, 105–106 infantile/congenital esotropiarelated, 106, 225 Snellen acuity, comparison with contrast acuity, 13 Snellen letters, 11–12, 109 Spectacles hypermetropic, for infantile/ congenital esotropia correction, 232

for hypermetropic accommodative esotropia correction, 244–246 indications for prescription of, 127, 128 polarized, as haploscopic devices, 77–78 prescription guidelines for, 522–524 strabismic deviation measurement through, 527 Spin test, 431, 442 Spiral of Tillaux, 30 Split-tendon lengthening procedure, superior oblique, 289, 414 Split-tendon transposition procedures Hummelsheim procedure, 353, 354, 355, 365, 369, 404, 405, 406, 419 Jensen procedure, 404, 405 Squinting to bright light. See Photophobia strabismus-related, 84 Starling’s length-tension curve, 388, 389, 390 Stereoacuity from binocular retinal ﬁelds, 75 from central ﬁeld, 75 high-grade, 81 quantiﬁcation of, 78 Stereoacuity testing, 76–80 contour, 77, 78–79 random dot, 79–80 Stereopsis intermittent exotropia surgeryrelated loss of, 274 normal development of, 7 Stereoscopic resolution, 78 Stereoscopic vision, 72, 74–75 Steroids, as myasthenia gravis treatment, 476–477 Stimulation, active, of amblyopic eyes, 132–133 Strabismus acquired as confusion cause, 177–178 prognosis for, 138–139 as amblyopia cause, 109, 110 ﬁxation preference testing for, 119–122 pathophysiologic mechanisms of, 110, 113 vertical prism testing for, 122–125 angle of, measurement of. See Ocular deviations, measurement of

index Strabismus (Continued) A-pattern deﬁnition of, 284 ET-pattern, 284 lamba-pattern, 286 treatment of, 287–289 XT-pattern, 284 basic concepts of, 84–102 comitant, 100 botulinum toxin treatment of, 421 surgical treatment of, 391 complex, deﬁnition of, 323 congenital incomitant, large regional suppression in, 188 prognosis for, 138–139 as cortical suppression cause, 107 cranial nerve III palsy-related, 362, 363 deﬁnition of, 84 dissociated, 370–379 distance measurements in, 3 divergent, most common form of, 266 duration of, 138–139 effect on visual development, 103, 107 horizontal, inferior oblique overaction associated with, 311 idiopathic, 85 incomitant, 100 congenital, large regional suppression in, 188 deﬁnition of, 323 extraocular muscle paresisrelated, 100, 101–102 left lateral rectus paresisrelated, 100, 101 management of, 332–334 right medial rectus recessionrelated, 391 intermittent, as binocular fusion indicator, 139 large-angle adjustment suture technique in, 396 depth perception in, 81 suppression scotomas associated with, 188, 189 Marcus Gunn jaw-winking-related, 468–469 myasthenia gravis-related, 477 occlusion therapy for, 130

555 paralytic, 85, 352–369 adjustment suture technique in, 396 aplasia of extraocular musclesrelated, 365–369 cranial nerve III palsy-related, 362–364 cranial nerve IV palsy-related, 362 cranial nerve VI palsy-related, 352–355 craniosynotosis-related, 369 differentiated from restrictive strabismus, 323–324, 327–332 Duane’s syndrome-related, 355–362 inferior oblique palsy-related, 364 Möbius syndrome-related, 364–365 sinus surgery-related, 365 primary deviation, 442 refractive error-related, 85 restrictive, 85 causes of, 326 congenital ﬁbrosis of the extraocular muscles -related, 339–340 differentiated from paralytic strabismus, 323–324, 327–332 double elevator palsy-related, 340–342 fat adherence syndromerelated, 334–336 glaucoma explant surgeryrelated, 349–351 Graves’ ophthalmology-related, 336–338 local anesthetics-related, 343, 345–346 monocular elevation deﬁcit syndrome-related, 340–342 myopic strabismus ﬁxusrelated, 351–252 orbital ﬂoor fracture-related, 342–345 retinal surgery-related, 346–349 in saccade initiation failure, 434, 455 secondary deviation, 442 sensory aspects of. See Sensory adaptations, to strabismus

556

index

Strabismus (Continued) small-angle, monoﬁxation syndrome associated with, 179, 201 as squinting cause, 84 torsional, rectus muscle transposition surgery for, 406–407 vertical, 87–88 V-pattern arrow, 285, 286 bilateral superior oblique paresis-related, 296, 297 craniosynostosis-related, 369 deﬁnition of, 284 ET-pattern, 284 treatment of, 287–289 XT-pattern, 284 Y-pattern, 285 Strabismus examination. See Motor examination, ocular Strabismus ﬁxus, 232, 339 acquired, 351 myopic, 351–352 Strabismus surgery, 388–422 complications of slipped or lost rectus muscle, 418–419 stretched insertion scar, 419 effect on astigmatic correction, 523 Faden procedure, 333, 399–402 inferior oblique muscle weakening procedures, 407–411 anterior transposition, 407–410 extirpation-denervation, 407 graded recessionanteriorization, 410–411 myotomy, 407 recession, 407, 408 muscle recession procedures, 388–396 adjustable suture technique in, 394–396 hang-back technique in, 393–394, 396 as incomitant strabismus treatment, 332 inferior oblique muscle, 311, 391, 407, 408 inferior rectus muscle, 37, 337 lateral rectus muscle, 274–275, 287, 288, 373 rectus muscle, 388–391

Starling’s length-tension curve in, 388, 389, 390 muscle shortening procedures, 396–399 plications, 396, 398–399 resections, 396, 397 tucks, 396, 397–398 muscle transposition procedures, 402–407 anteriorization, inferior oblique, 45–47, 311–312, 327, 407–410 complications of, 406 of horizontal rectus muscle, 287–288, 289, 308, 403, 407 inferior oblique anteriorization, 45–47, 311–312, 327, 373, 407–410 for rectus muscle palsy, 404–406 for small vertical deviations, 403 for torsion, 406–407 in myotonic dystrophy, 488 recession-resection (“R and R”) procedure, 399 superior oblique muscle tightening procedures, 411–414 full-tendon tuck or plication, 413–414 Harada-Ito procedures, 412–413 superior oblique muscle weakening procedures, 414–418 dissociated vertical deviationexacerbating effect of, 308, 414–418 tenotomy, 415–416 for unilateral inferior oblique paresis, 305–306 Wright superior oblique tendon expander, 415, 416–418 Stroke, as dorsal midbrain syndrome cause, 436, 437 Superior colliculi, 426 Superior oblique muscle actions of, 27, 40 anatomic insertion of, 27 anatomy of, 40–42 arc of contact of, 27 ﬁeld of action of, 28, 29 length of, 27 origin of, 27

index Superior oblique muscle (Continued) palsies of abnormal head posturing associated with, 374 traumatic, 304 vertical fusion vergence amplitude in, 98 pareses of, 294–299 bilateral, 296–297, 304, 305 Brown’s syndrome-related, 319 congenital, 295, 300–302 as “fallen eye” cause, 297–298 head tilt associated with, 295 head tilt test in, 294–295, 296 infantile esotropia associated with, 220 as inhibitional palsy of the contralateral antagonist, 298–299 right, 291 tenotomy- or tenectomyrelated, 317 traumatic, 296, 297, 299–300 treatment of, 302–304, 305 unilateral, 294–295, 296, 297, 303 V-pattern, 310 tendon ﬁbers of, 41–42 underaction of, craniosynostosisrelated, 369 Superior oblique muscle overaction, 306–308 adduction elevation deﬁcits associated with, 306, 316 A-(lambda) pattern, 306, 307 with A- or V-pattern strabismus, 288 with binocular vision, 288–289 clinical features of, 306–307 differential diagnosis of, 306, 307 inferior oblique paresis versus, 299 intermittent exotropia-related, 275 isolated inferior oblique paresisrelated, 304–305, 308 superior oblique muscle weakening procedures for, 414 treatment of. See Superior oblique muscle weakening procedures Superior oblique muscle tightening procedures, 411–414 full-tendon tuck or plication, 413–414 Harada-Ito procedures, 412–413 Superior oblique muscle tuck, 303–304

557

Superior oblique muscle weakening procedures, 308, 414–418 dissociated vertical deviationexacerbating effect of, 308 tenotomy, 415–416 for unilateral inferior oblique paresis, 305–306 Wright superior oblique tendon expander, 275–276, 289, 305–306, 308, 391, 415, 416–418 Superior oblique tendon anatomic relationship with trochlea, 42, 43, 44 functional divisions of, 411, 412 tight, as Brown’s syndrome cause, 315 Superior oblique tendon lengthening procedures as congenital Brown’s syndrome treatment, 317 split-tendon, 289, 414 Superior oblique tendon recession, 391 Superior oblique tendon silicone expander. See Wright superior oblique tendon silicone expander Superior oblique tendon transfer, as cranial nerve II palsy treatment, 363 Superior rectus muscle actions of, 27, 36 anatomic insertion of, 27 anatomic relationship with levator palpebrae, 36 anatomy of, 35, 36, 37 arc of contact of, 27 length of, 27 Marcus Gunn jaw-winking-related palsy of, 468–469 origin of, 27 transposition of, 407 weakness of, 439 yoke muscle function of, 66 Superior rectus muscle recession as dissociated vertical deviation treatment, 373 as lid ﬁssure widening cause, 36 as upper lid retraction cause, 36 Superior rectus muscle resection, as lid ﬁssure narrowing cause, 36 Suppression, tests for, 212–216 amblyoscope testing, 206 red ﬁlter test, 193, 194, 195–196 vertical prism red ﬁlter test, 196, 197, 198 Supraduction, 27

558 Supranuclear eye movements, 423–440 disorders of, 432–440 physiology and clinical evaluation of, 424–431 Supraversion, 67 Sursumduction, 27 Swinging ﬂashlight test, 15–16 Sylvian aqueduct sign, 435 Syndactyly, Möbius syndrome-related, 364 Synergistic divergence, 356, 357, 359, 466–467 T TCU (City University Color Vision) Test, 13 Tenacious proximal fusion, 99 10 diopter ﬁxation test, 122–125 Tenectomy, as congenital Brown’s syndrome treatment, 317 Tenon’s capsule, 52–58 categories of anterior Tenon’s capsule, 53–55 check ligaments, 54, 57–58 intermuscular septum, 53, 54 posterior Tenon’s capsule, 55–57 deﬁnition of, 52 in fat adherence, 334, 335 scarring of, 325 surgery-related tears of, 336 Tenotomy as congenital Brown’s syndrome treatment, 317 superior oblique, 308 as superior oblique paresis cause, 302 Tensilon test, 448, 474–475, 479 contraindications to, 474–475 Thalidomide, 359 Thorazine (DPT), 4, 5 Three-step test, 291, 292–294 Thymoma, 476 Thyroid myopathy. See also Graves’ disease/ophthalmology intraocular pressure increase in, 331 as ocular restriction cause, 325, 326 Titmus test, 78, 79 Tonometry and tonometers, 16–17 handheld, 3 Tonopen, 17

index Torsion assessment of, 165, 167–168 deﬁnition of, 88 subjective, 88 Torticollis, 373–374 ocular, 374, 375, 378–379 Toxocara canis, 147 Transposition procedures. See Muscle transposition procedures Trochlea anatomic relationship with superior oblique muscle, 40, 41 superior oblique tendon, 42, 43, 44 anatomy of, 41, 42, 45 histology of, 43 pathology of, as Brown’s syndrome cause, 315, 316, 319 Trochlear nerve. See Cranial nerve IV Trochleitis, 315 Tropias, 84 cover/uncover test for, 150–151 differentiated from phorias, 204 greater than 10 prism diopters, 89 less than 10 prism diopters, 89 Tropicamide, 18, 19 as cycloplegia agent, 521 Trust, in physician-patient relationship, 3 Tucks, 396, 397–398 Tumbling E, 3 28-diopter lens, 3 U Ultraviolet protection, 524 V Varicella virus infection, as GuillainBarré syndrome cause, 457–458 Vectographic tests, 212, 213–214 Vergences, 81–83, 425, 430, 431 convergence, 82–83 disjunctive nature of, 82 divergence, 83 in dorsal midbrain syndrome, 436 fusional amplitudes in, 95–96, 98 prism-induced, 95 insufﬁciency of, 474 vertical, 83 normal amplitude of, 96 Versions, 65, 67, 141–143

index Vertical gaze, transient abnormalities of, 438–439 Vertical prism red ﬁlter test, 196, 197, 198 Vertical prism test, 122–125 Vertical rectus muscles. See also Inferior rectus muscle; Superior rectus muscle action of, 27–28 actions of, 35–36 anatomic relationship with inferior oblique muscle, 40, 41 anatomy of, 35–38 palsy of, three-step test for, 292 removal of, as hypoperfusion cause, 59, 60 transposition of, 406, 407 as cranial nerve VI palsy treatment, 345 Vertical retraction syndrome, 339, 467–468 Vestibular apparatus, role in eye movements, 424–425 Vestibular-ocular reﬂex (VOR), 65 assessment of, 425, 431 cancellation of, 425 dampening of, 9 in saccade initiation failure, 434 Vieth-Müller circle, 71, 72 Viral infections as cranial nerve VI palsy cause, 445 as Guillain-Barré syndrome cause, 457–458 Vision screening, 125–129 red reﬂex test in, 125, 126–129 Vistech wall chart, 14 Visual acuity at birth, 103 development of age-related improvement in, 103, 104 critical period of, 103 requirements for, 104, 105 neonatal development of, 103 Visual acuity testing in latent nystagmus, 123, 125 preverbal, 6–11, 140 verbal, 11–13, 140–141

559

Visual axis, 24, 25 Visual development, 103–137 abnormal, 107–125 cortical sensory adaptation in, 111 cortical suppression-related, 107–108 critical period for, 109 developmental milestones in, 106–107 normal, 7, 103–105 binocular, 104–105 cortical sensory adaptation in, 111 monocular, 103 Visual evoked potentials (VEPs) pattern (PVEP), 9, 10–11 effect of cortical suppression on, 107, 108 in strabismus-related cortical activity suppression, 190 Visual ﬁeld testing, 12 automated, 12 Visual loss/impairment, unilateral, as sensory exotropia cause, 280–281 Visual maturation, delayed, 106–107 Visuscope, 119 W Worth 4-dot test, 180, 182 in large regional suppression, 189 as partial haploscopic test, 205 stimulus angle for, 202 Wright, Kenneth W., 118 Wright ﬁgures, 3, 11, 118, 141 Wright rectus muscle plication, 59, 60, 398–399 Wright superior oblique tendon silicone expander, 275–276, 289, 305–306, 308, 391, 415, 416–418 as Brown’s syndrome treatment, 313, 317–319 X X-pattern strabismus, 286–287 Y Y axis of Flick, 88 Y-splitting procedure, 362