Food Irradiation Research and Technology

Food Irradiation Research and Technology

The IFT Press series reflects the mission of the Institute of Food Technologists— advancing the science and technology of food through the exchange of knowledge. Developed in partnership with Blackwell Publishing, IFT Press books serve as essential textbooks for academic programs and as leading edge handbooks for industrial application and reference. Crafted through rigorous peer review and meticulous research, IFT Press publications represent the latest, most significant resources available to food scientists and related agriculture professionals worldwide.

IFT Book Communications Committee Ruth M. Patrick Dennis R. Heldman Theron W. Downes Joseph H. Hotchkiss Marianne H. Gillette Alina S. Szczesniak Mark Barrett Neil H. Mermelstein Karen Banasiak

IFT Press Editorial Advisory Board Malcolm C. Bourne Fergus M. Clydesdale Dietrich Knorr Theodore P. Labuza Thomas J. Montville S. Suzanne Nielsen Martin R. Okos Michael W. Pariza Barbara J. Petersen David S. Reid Sam Saguy Herbert Stone Kenneth R. Swartzel

Food Irradiation Research and Technology

EDITORS

Christopher H. Sommers • Xuetong Fan

Titles in the IFT Press series • Accelerating New Food Product Design and Development (Jacqueline H.P. Beckley, J.C. Huang, Elizabeth J. Topp, M. Michele Foley, and Witoon Prinyawiwatkul) • Biofilms in the Food Environment (Hans P. Blaschek, Hua Wang, and Meredith E.Agle) • Food Carbohydrate Chemistry (Ronald E.Wrolstad) • Food Irradiation Research and Technology (Christopher H. Sommers and Xuetong Fan) • Foodborne Pathogens in the Food Processing Environment: Sources, Detection and Control (Sadhana Ravishankar and Vijay K. Juneja) • High Pressure Processing of Foods (Christopher J. Doona, C. Patrick Dunne, and Florence E. Feeherry) • Hydrocolloids in Food Processing (Thomas R. Laaman) • Microbiology and Technology of Fermented Foods (Robert W. Hutkins) • Multivariate and Probabilistic Analyses of Sensory Science Problems (JeanFrancois Meullenet, Rui Xiong, and Chris Findlay) • Nondestructive Testing of Food Quality (Joseph Irudayaraj and Christoph Reh) • Nonthermal Processing Technologies for Food (Howard Q. Zhang, Gustavo V. Barbosa-Canovas, V.M. Balasubramaniam, Editors; C. Patrick Dunne, Daniel F. Farkas, James T.C.Yuan,Associate Editors) • Packaging for Nonthermal Processing of Food (J. H. Han) • Preharvest and Postharvest Food Safety: Contemporary Issues and Future Directions (Ross C. Beier, Suresh D. Pillai, and Timothy D. Phillips, Editors; Richard L. Ziprin,Associate Editor) • Regulation of Functional Foods and Nutraceuticals: A Global Perspective (Clare M. Hasler) • Sensory and Consumer Research in Food Product Design and Development (Howard R. Moskowitz, Jacqueline H. Beckley, and Anna V.A. Resurreccion) • Thermal Processing of Foods: Control and Automation (K.P. Sandeep) • Water Activity in Foods: Fundamentals and Applications (Gustavo V. BarbosaCanovas,Anthony J. Fontana Jr., Shelly J. Schmidt, and Theodore P. Labuza)

Christopher Sommers is a research microbiologist, and Xuetong Fan is a research food technologist. Both work for the Food Safety Intervention Technologies Research Unit, USDA-ARS-Eastern Regional Research Center, Wyndmoor, Pennsylvania. Sommers and Fan were co-moderators of the IFT symposium from which this book arose. Copyright © Blackwell Publishing and the Institute of Food Technologists 2006 All rights reserved Blackwell Publishing Professional 2121 State Avenue,Ames, Iowa 50014, USA Orders: Office: Fax: Web site:

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Blackwell Publishing Ltd 9600 Garsington Road, Oxford OX4 2DQ, UK Tel.: +44 (0)1865 776868 Blackwell Publishing Asia 550 Swanston Street, Carlton,Victoria 3053,Australia Tel.: +61 (0)3 8359 1011 Authorization to photocopy items for internal or personal use, or the internal or personal use of specific clients, is granted by Blackwell Publishing, provided that the base fee of $.10 per copy is paid directly to the Copyright Clearance Center, 222 Rosewood Drive, Danvers, MA 01923. For those organizations that have been granted a photocopy license by CCC, a separate system of payments has been arranged.The fee codes for users of the Transactional Reporting Service are ISBN13: 978-0-8138-0882-6; ISBN-10: 0-8138-0882-0/2006 $.10. First edition, 2006 Library of Congress Cataloging-in-Publication Data Food irradiation research and technology/edited by Christopher H. Sommers and Xuetong Fan.—1st ed. p. cm.—(IFT Press series) Includes bibliographical references and index. ISBN-13: 978-0-8138-0882-6 (alk. paper) ISBN-10: 0-8138-0882-0 (alk. paper) 1. Radiation preservation of food—Research. 2. Irradiated beef. I. Sommers, Christopher H. II. Fan, Xuetong. III. Series. TP371.8.F676 2006 664⬘.0288—dc22 2005028697 The last digit is the print number: 9 8 7 6 5 4 3 2 1

CONTENTS List of Contributors Preface

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Chapter 1. Introduction: Food Irradiation Moving On Joseph Borsa

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Chapter 2. Advances in Gamma Ray, Electron Beam, and X-ray Technologies for Food Irradiation Marshall R. Cleland

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Chapter 3. Regulation of Irradiated Foods and Packaging George H. Pauli

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Chapter 4. Toxicological Safety of Irradiated Foods Christopher H. Sommers, Henry Delincée, J. Scott Smith, and Eric Marchioni

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Chapter 5. Consumer Acceptance and Marketing of Irradiated Foods Ronald F. Eustice and Christine M. Bruhn

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Chapter 6. Detection of Irradiated Foods Eric Marchioni

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Chapter 7. Dosimetry for Food Processing and Research Applications Kishor Mehta and Kevin O’Hara

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Chapter 8. Mechanisms and Prevention of Quality Changes in Meat by Irradiation Doug U. Ahn and E.J. Lee

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Chapter 9. Irradiation as a Phytosanitary Treatment for Fresh 143 Horticultural Commodities: Research and Regulations Peter A. Follett and Robert L. Griffin

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Contents

Chapter 10. Low-Dose Irradiation of Fresh and Fresh-Cut Produce: Safety, Sensory, and Shelf Life Brendan A. Niemira and Xuetong Fan

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Chapter 11. Irradiation of Seafood with a Particular Emphasis 185 on Listeria monocytogenes in Ready-to-Eat Products Denise M. Foley Chapter 12. Ionizing Radiation of Eggs I. Álvarez, B.A. Niemira, X. Fan, and C.H. Sommers

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Chapter 13. Irradiation Treatment of Nuts Akua Kwakwa and Anuradha Prakash

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Chapter 14. Irradiated Ground Beef for the National School Lunch Program Xuetong Fan

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Chapter 15. Potential Applications of Ionizing Radiation Myung-Woo Byun, Cheorun Jo, and Ju-Woon Lee

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Chapter 16. A Future Uncertain: Food Irradiation from a Legal Perspective Denis W. Stearns

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Chapter 17. Technical Challenges and Research Directions in Electronic Food Pasteurization Suresh D. Pillai, Les Braby, and Joe Maxim

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Index

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LIST OF CONTRIBUTORS Doug U. Ahn Animal Science Department, Iowa State University,Ames, IA 50011, U.S.A. Phone: (515) 294-6595. E-mail: [email protected] Chapter 8 Ígnacio Álvarez Tecnología de los Alimentos, Facultad de Veterinaria, University of Zaragoza, 50013, Zaragoza, Spain. Phone: +34976761581. E-mail: [email protected] Chapter 12 Joseph Borsa MDS Nordion, Ottawa, Canada K2K 1X8, Canada. Phone: (613) 592-2790. E-mail: [email protected] Chapter 1 Les Braby National Center for Electron Beam Food Research, Institute of Food Science & Engineering,Texas A&M University, College Station,TX 77845, U.S.A. Phone: (979) 862-1798. E-mail: [email protected] Chapter 17 Christine M. Bruhn Center for Consumer Research, Department of Food Science & Technology, University of California, Davis, CA 95616, U.S.A. Phone: (530) 752-2774. E-mail: [email protected] Chapter 5 Myung-Woo Byun Radiation Food Science & Biotechnology Team,Advanced Radiation Technology Institute, Korea Atomic Energy Research Institute, 1266, Sinjeong-dong, Jeongeup, 580-185, Republic of Korea. Phone: (82) 63 570 3200. E-mail: [email protected] Chapter 15

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List of Contributors

Marshall R. Cleland IBA Techninogy Group, IBA-RDI E-Beam X-Ray Solutions, Edgewood, NY 11717, U.S.A. Phone: (631) 979-8718. E-mail: [email protected] Chapter 2 Henry Delincée Federal Research Centre for Nutrition and Food, Institute of Nutritional Physiology, Haid-und-Neu-Str. 9, 76131 Karlsruhe, Germany. Phone: +49 721-6625-401. E-mail: [email protected] Chapter 4 Ronald F. Eustice Executive Director, Minnesota Beef Council, 2950 Metro Drive # 102, Minneapolis, MN 55425, U.S.A. Phone: (952) 854-6980. E-mail: [email protected] Chapter 5 Xuetong Fan Eastern Regional Research Center,Agricultural Research Service, U.S. Department of Agriculture,Wyndmoor, PA 19038, U.S.A. Phone: (215) 836-3785. E-mail: [email protected] Chapter 10, Chapter 12, Chapter 14 Denise M. Foley Department of Biological Sciences, Chapman University, One University Drive, Orange, CA 92866, U.S.A. Phone: (714) 628-7209. E-mail: [email protected] Chapter 11 Peter A. Follett USDA,ARS, Pacific Basin Agriculture Research Center, Hilo, HI 96720, U.S.A. Phone: (808) 959-5470. E-mail: [email protected] Chapter 9 Robert L. Griffin USDA,APHIS, Plant Epidemiology and Risk Analysis Laboratory, Raleigh, NC 27606, U.S.A. Phone: (770) 228-7303. E-mail: [email protected] Chapter 9

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Cheorun Jo Radiation Food Science & Biotechnology Team,Advanced Radiation Technology Institute, Korea Atomic Energy Research Institute, 1266, Sinjeong-dong, Jeongeup, 580-185, Republic of Korea. Phone: (82) 63 570 3200. E-mail: [email protected]. Chapter 15 Akua Kwakwa Department of Physical Sciences, Chapman University One University Drive, Orange, CA 92866, U.S.A. Phone: (714) 744-7826. Chapter 13 E.J. Lee Animal Science Department, Iowa State University,Ames, IA 50011, U.S.A. Chapter 8 Ju-Woon Lee Radiation Food Science & Biotechnology Team,Advanced Radiation Technology Institute, Korea Atomic Energy Research Institute, 1266, Sinjeong-dong, Jeongeup, 580-185, Republic of Korea. Phone: (82) 63 570 3200 Chapter 15 Eric Marchioni Laboratoire de Chimie Analytique et Sciences de l’Aliment (UMR 7512), Faculté de Pharmacie, 74 Route du Rhin, F-67400 Illkirch Graffenstaden. Phone: 03.88.67.69.44. E-mail: [email protected] Chapter 4, Chapter 6 Joe Maxim National Center for Electron Beam Food Research, Institute of Food Science & Engineering,Texas A&M University, College Station,TX 77845, U.S.A. Phone: (979) 862-2036. E-mail: [email protected] Chapter 17 Kishor Mehta Senior Scientist Emeritus, IAEA, Bruenner Strasse 133-3-29,A-1210, Vienna,Austria. Phone: (43) 1-22 46 099. E-mail: [email protected] Chapter 7

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List of Contributors

Brendan A. Niemira Eastern Regional Research Center,Agricultural Research Service, U.S. Department of Agriculture,Wyndmoor, PA 19038, U.S.A. Phone: (215) 836-3784. E-mail: [email protected] Chapter 10, Chapter 12 Kevin O’Hara MDS Nordion, 447 March Road, Ottawa Ontario, K2K 1X8, Canada. Phone: (613) 592-3400 Ext. 2524. E-mail: [email protected] Chapter 7 George H. Pauli Associate Director for Science and Policy, HFS-205, Office of Food Additive Safety, Center for Food Safety and Applied Nutrition, Food and Drug Administration, 5100 Paint Branch Parkway, College Park, MD 20740-3835, U.S.A. Phone: (202) 418-3090. E-mail: [email protected] Chapter 3 Suresh D. Pillai National Center for Electron Beam Food Research, Institute of Food Science & Engineering,Texas A&M University, College Station,TX 77845, U.S.A. Phone: (979) 845-1921. E-mail: [email protected] Chapter 17 Anuradha Prakash Department of Physical Sciences, Chapman University, One University Drive, Orange, CA 92866, U.S.A. Phone: (714) 744-7895. E-mail: [email protected] Chapter 13 J. Scott Smith The Food Science Institute,Animal Science and Industry, 2008 Call Hall, Kansas State University, Manattan, KS 66506, U.S.A. Phone: (785) 532-5681. E-mail: [email protected] Chapter 4

List of Contributors Christopher H. Sommers U.S. Department of Agriculture,Agricultural Research Service, Eastern Regional Research Center, 600 East Mermaid Lane,Wyndmoor, PA 19038, U.S.A. Phone: (215) 836-3754. E-mail: [email protected] Chapter 4, Chapter 12 Denis W. Stearns Marler Clark,Attoneys at Law, Seattle,WA 98104, U.S.A. Phone: (206) 346-1892. E-mail: [email protected] Chapter 16

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PREFACE Christopher H. Sommers, Ph.D.

Food Irradiation Is Already Here* At present there are approximately 60 commercial irradiation facilities operating in the United States. Many food scientists and technologists are unaware that the “food irradiation industry” is only a small part of a much larger industrial group dedicated to radiation processing. Every two years the International Meeting on Radiation Processing (IMRP) convenes, and presentations are made on the radiation processing of materials, medical and pharmaceutical products, cosmetics, vaccines, advances in irradiation technology and facilities, radiation dosimetry, and more. Published in Radiation Physics and Chemistry (Vol. 71[1-2], 2004), the collection of papers presented at IMRP-2003 in Chicago is 606 pages long and weighs in at 1 kilogram. It contains publications on the irradiation of spices, nutraceuticals, seafood, meat and poultry, and fruits and vegetables for inactivation of bacterial pathogens and parasites and phytosanitary purposes. Irradiation of food and agricultural products, as part of the larger radiation processing industry, is currently allowed by about 60 countries around the globe. In 1997, the U.S. Food and Drug Administration approved the use of ionizing radiation to inactivate pathogenic bacteria in red meat.Although some scientists and public health officials are frustrated by the slow pace with which irradiated ground beef is penetrating the U.S. market, I question whether that frustration is warranted. Many food scientists forget that it took almost 50 years for pasteurized milk to be accepted by the public in the United States. At the 2005 IFT Annual Meeting and Food Expo in Las Vegas, Ron Eustice of the Minnesota Beef Council reminded us that processors such as Sadex, Inc. (Sioux City, IA), Food Technology *Edited and reprinted from Sommers, C.H. Food Irradiation Is Already Here. Food Technology 58 (4):22. 2004.

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Services (Mulberry, FL), and the Institute for Food Science and Engineering (Texas A&M University) are still supplying irradiated meat and poultry to thousands of stores across the United States, even after the demise of Surebeam Corporation. In September 2004, Rochester, NY–based Wegman’s Food Markets, Inc. announced that Huisken BeSure™ irradiated beef patties are available at supermarkets in New York, New Jersey, and Pennsylvania. Thus, irradiated meat and poultry have not gone away. Although introduced too late in the 2004 school year to allow orders to be placed, irradiated ground beef was made available, on a voluntary basis, as part of the National School Lunch Program administered by the USDA’s Agricultural Marketing Service (AMS) and Food and Nutrition Service (FNS).Within the last year, the Child Nutrition Improvement and Integrity Act was amended to codify the procurement, labeling, and educational programs already developed by FNS and AMS for irradiated ground beef. Most important, Congress mandated that “States and school food service authorities are provided model procedures for providing factual information on the science and evidence regarding irradiation technology. . . .” The word “factual” is critical to the education process concerning irradiated foods. At USDA ARS’s Eastern Regional Research Center in Wyndmoor, PA, we investigate an array of thermal and nonthermal intervention technologies to improve the microbiological safety and quality of foods; such technologies include high-pressure processing, radio frequency electric fields, competitive microbial exclusion, UHT pasteurization, and vacuum-steam-vacuum surface treatment. In contrast to the private sector, we do not promote the use of specific technologies, such as irradiation, over that of others that would achieve the same objective. In other words, we are interested in objectively and comparatively evaluating the efficacy of a whole range of intervention technologies. That being said, what are the facts surrounding irradiation of ground beef? (1) Irradiation can inactivate pathogenic bacteria occasionally found in ground beef such as E. coli O157:H7, Salmonella, Staphylococcus aureus, and Listeria monocytogenes; (2) irradiation of food, including ground beef, does not make food radioactive; (3) irradiation, when used appropriately, does not change the aroma, taste, aftertaste, texture, or overall liking of ground beef, including frozen ground beef supplied as part of the National School Lunch Program; (4) there is no detectable increase in the risk of cancer associated with long-term consumption of radiation-pasteurized meat as determined by multispecies, multigeneration feeding studies conducted in animals; (5) irradiated ground beef is nutritious and wholesome; and (6) irradiation is effective

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only as part of a comprehensive program designed to improve the microbiological safety of ground beef, not to “clean up” unacceptable product. As scientists and technologists, we have a responsibility to ensure that educational materials provided to the public regarding food safety and processing technologies are based on sound science and fact, as opposed to misconceptions. Food Irradiation Research and Technology meets that goal.

Acknowledgements We would like to thank the Institute of Food Technologists and the IFT Non-Thermal Processing Division for their support, and Mark Barrett and Dede Pedersen for the guidance and patience during the completion of this work. We would also thank the contributors and authors to this book, who are experts in the field of food irradiation, chemistry, physics, consumer acceptance and education, and the law as applies to foodborne illness.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Food Irradiation Research and Technology

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 1 INTRODUCTION: FOOD IRRADIATION MOVING ON Joseph Borsa, Ph.D.

Introduction There’s an old Chinese proverb that says, “May you live in interesting times.”With respect to food irradiation (Borsa 2000), today’s proponents and other observers of this technology have good reason to feel that indeed these are interesting times in this unfolding story. Studied intensively for more than half a century, and approved in some 50 countries around the globe for a wide variety of food products (ICGFI 2005), irradiation has been widely used for spices and other food ingredients for many years, but for perishables (meat and produce) it is just now emerging into a significant commercial reality.This essay focuses primarily on these emerging applications, in which just in the past half dozen years or so the changes in what we might call the food irradiation landscape have been dramatic and at times go well beyond that. These changes have been most pronounced in the United States but the effects are beginning to be felt in other countries around the globe as well. In the United States from basically a standing start at the beginning of this recent period, but powered by a high level of entrepreneurial energy and zeal, commercialization of irradiation technology in the food industry accelerated rapidly to reach heights far beyond anything previously achieved. Almost overnight, irradiated products appeared in literally thousands of retail and foodservice outlets (SureBeam 2001). Investors took notice (Titan Corp 2001) and millions of dollars were raised for ventures targeting the opportunity presented by the very real needs recognized in food safety (Osterholm and Norgan 2004) and quarantine security (IAEA 2004). The fact that those needs are evident all over the world added to the investment appeal. In these positive circumstances, 3

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interest in food irradiation rapidly escalated, giving rise to an exciting play in the investment world. Unfortunately, in 2004 a major business miscalculation intervened and this nascent industry suffered a significant setback just as it appeared to be getting over the hurdles associated with its launch. Not surprisingly, and to the great satisfaction of the skeptics and antitechnology activists, unreasonable expectations had exceeded the actual pace of adoption, especially by the major food processors, and the simple but inexorable math of the business world led SureBeam™, the most prominent player in the field, to declare bankruptcy (Egerstrom 2004).This failure caused considerable consternation and uncertainty in the fledgling industry, raising concerns as to whether it would survive the setback. Now, more than a year later and with the dust largely settled, it appears that emerging from this uncertainty is a restructured food irradiation industry that is gradually regaining momentum.The fundamental benefits offered by the technology remain the same (Olson 2004) and the new path forward, although lacking the brash boldness and dash of the SureBeam™ approach, offers prospects for a more sustainable long-term future.

Two Tracks Going Forward Two major separate driving forces are moving adoption of food irradiation forward. One is the need to effect microbial reduction, primarily for purposes of food safety enhancement. This need is associated especially with those foods that are derived from animals, although similar food safety needs are increasingly being recognized for fresh fruits and vegetables (Sewall and Farber 2001). Shelf-life extension constitutes a significant additional incentive for adoption of this technology, and in some specific applications it may serve as the primary benefit being sought. The second major driver is the need for an effective and environmentally friendly technology to disinfest fruits and vegetables for quarantine security purposes associated with interregional trade (NAPPO 2003). These two main driving forces translate into two distinct business opportunities on which the current implementation activities are centered. The Food Safety Track Irradiation with ionizing energy is very effective in killing many of the common microbial pathogens such as E. coli O157:H7, Listeria monocytogenes, Salmonella spp. and Vibrio spp., among others, that are significant contributors to foodborne illness. A major advantage of irradiation

Introduction: Food Irradiation Moving On

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for this purpose is that the food can be processed after it has been sealed in its final packaging, thereby reducing or eliminating entirely the possibility of recontamination following this treatment. This unique operational capability makes irradiation particularly suitable for (cold) pasteurization of ready-to-eat foods, such as hot dogs and other deli items, that are at risk of contamination with Listeria monocytogenes during postprocess slicing and packaging operations. How does irradiation fit into the overall food safety strategy, based on Hazard Analysis Critical Control Point (HACCP), which is now the dominant food safety paradigm in the food industry? Although the incidence of positive samples for both E. coli O157:H7 (USDA 2005) and Listeria monocytogenes (USDA 2003) has declined significantly since HACCP was made mandatory in the late 1990s, the need for further improvement remains.A simple calculation puts this into useful perspective.The latest sampling statistics from USDA-FSIS indicate that the incidence of ground beef samples testing positive for contamination with E. coli O157:H7 stands at 0.17% (USDA 2004). This translates into roughly 17 million pounds of such contaminated ground meat presumably randomly interspersed through the approximately 10 billion pounds of this product consumed annually in the United States. Expressed in terms of commonly consumed units of ground beef, this amount represents some 68 million average-size hamburger patties that are contaminated by this pathogen and which therefore have the potential to cause illness in consumers. Of course, this scenario is for only one pathogen; there are others, including some newly emerging ones, which multiply the risk. In the present situation eating such product with the documented levels of contamination becomes a statistical game of chance as to whether one gets exposed to this pathogen or not. Although the probability of falling ill due to consumption of a randomly selected hamburger borders on the infinitesimally small, this is one of those situations in which a very small probability multiplied by the very large number of people at risk amounts to a significant number of seriously sick people, as attested to by CDC statistics (Mead and others 1999). Of course, for those unlucky enough to actually become sick, or whose child gets hemolytic uremic syndrome (HUS), the talk of probabilities becomes irrelevant (STOP 2003).Thus the need for further improvement is still very real.The “zero tolerance” regulatory policy in effect for this pathogen (USDA 1999) reflects the seriousness of the hazard. In the context of HACCP irradiation is an excellent CCP (Molins and others 2001) for E. coli O157:H7 and other bacterial pathogens in ground beef and similar products. Its use would reduce the probability of contamination in the finished product by several orders of magnitude, de-

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pending on the specifics of any particular application. No other technology exists that can offer the convenience of processing in the final shipping cases, and even on pallets, while still treating every last gram of product to a standard that essentially guarantees absence of the target pathogen. Irradiation can offer to solid and semi-solid foods such as meat, poultry, and fish the same benefits that thermal pasteurization has brought to milk and other liquid products. In the past two years, since SureBeam™’s failure, two new irradiation plants for processing food for the purpose of microbial reduction have been commissioned in the United States. Of course, the ultimate success of these ventures will be decided in the market place, subject to all the realities, scrutiny, and judgments of the business world. On this basis it seems safe to predict that the days ahead will continue to provide “interesting times.” The Disinfestation Track Growth in international trade of agricultural products, especially tropical fruits and vegetables, is seen as a foundation component of the economic development strategy of many underdeveloped countries (World Trade Organization 2001). Disinfestation technology for quarantine security purposes is a critical enabler for such trade in agricultural products (Henson and Loader 2001). Currently, fumigation with methyl bromide is the predominant technology used for this purpose. However, the continuing availability of methyl bromide for this purpose is an open question, due to its ozone depleting potential. An international agreement (Montreal Protocol) is in effect to phase out the use of this chemical because of this negative effect on the environment (UNDP 2002). In addition, methyl bromide is phytotoxic to some commonly traded fruits and vegetables (Hallman 1998), bringing further pressure to bear to find a suitable alternative. Irradiation is increasingly being recognized as an excellent agent for disinfestation purposes, and there is considerable interest around the world in bringing this potential into reality. USDA-APHIS is playing a leading role in the effort to put in place the regulatory infrastructure needed to allow its use for products imported into the United States, as well as for export of American horticultural products. Success has already been achieved for irradiated products routinely being shipped from Hawaii to mainland United States (Hawaii Pride 2005). Efforts currently under way should lead, in the relatively short term, to expansion of the list of U.S. trading partner countries for which irradiation will be accepted as a suitable disinfestation measure for products shipped between them. It can be anticipated that successful establishment of irradiation as a quarantine se-

Introduction: Food Irradiation Moving On

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curity technology for trade involving the United States will rapidly lead to its use for this purpose in trade involving other trading partners.The recent commencement of shipment of irradiated Australian fruit to New Zealand (TVNZ 2004) represents a first step along this path. Currently, besides the Hawaiian and Australian/New Zealand examples, there is interest in and movement toward implementation of irradiation disinfestation as part of a trade-enabling infrastructure in several countries in different regions around the world, including the Asia-Pacific group and Latin America. The future for irradiation in this application looks bright indeed.

Bumps Still Remain on the Road Ahead Although implementation of food irradiation has taken great strides forward and is building momentum, it has not yet reached a condition of clear sailing. Several troublesome hindrances remain, which need to be addressed. On the regulatory front, much remains to be done, even in the United States, where most of the implementation progress to date has taken place. Specifically, petitions for clearance of irradiation for several categories of food that could benefit from this treatment continue to languish somewhere in the evaluation process.These include petitions for readyto-eat foods and for seafood. Elsewhere, an encouraging sign is that in some parts of the world, as in Brazil (ICGFI 2005), the authorities have granted blanket approval for irradiation of all foods, consistent with Codex Alimentarius recommendations (Codex 2003). Perhaps this will encourage other member states of Codex Alimentarius to base their national regulations for food irradiation on the international standard to which they are party. It seems likely that as food irradiation registers more and more successes, countries currently on the sidelines will join the growing movement toward greater acceptance and utilization of this powerful technology. Regulatory requirements for the labeling of foods that have been irradiated remain a deterrent to some processors who would otherwise use it on their products. This issue has been under review for several years now, but to date no suitable alternative has been put forth that would satisfy both the needs of industry to inform but not alarm consumers, and the consumers’ right to know.Also very important is the need to extend the list of clearances for irradiation of food packaging materials, to include more of the common modern polymers and films (ICGFI 2005). At present there is a major logistical impediment, stemming from the

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scarcity of processing capacity within reach of many food manufacturers that are interested in using irradiation.This difficulty can be alleviated only by building new capacity in strategic locations to provide easy access for those wishing to use it. Installation of contract service irradiators in distribution centers and cold storage warehouses that serve many clients would be a logical and cost-effective approach to meeting this logistical need. Such locations have the advantage of easy and convenient access for their clients without incurring any additional transportation costs. New irradiation systems currently available (Stichelbaut and Herer 2004) that can process fully loaded pallets of food allow seamless interfacing between the irradiation facility and the existing warehouse, distribution, and transportation networks that use pallets as the basic unit of product handling. Another challenge is that with some products the maximum dose that can be tolerated without sensory degradation is low enough that it can be difficult to effect the wanted benefit to the extent desired. Excellent research progress in improving the effectiveness of irradiation in such difficult cases is being made. Different approaches involve one or more of increasing the product tolerance to radiation (Kalsec 2005), increasing the sensitivity of pathogens to radiation so that lower doses can effect the needed kill (Chiasson and others 2004), and improvements to irradiator design permitting the delivery of more uniform dose distributions in product stacks (Stichelbaut and Herer 2004), thereby reducing the regions of overdose wherein the sensory degradation is most likely to occur.These and other technical issues will undoubtedly serve as the focus of research at universities and other institutions for some time to come.

Summary Implementation of food irradiation continues to move forward. The biggest gains are happening in the United States, but progress is being made in other parts of the world as well. Both the food safety and the disinfestation applications are growing, with the disinfestation application being especially active. It seems likely that this expansion will continue for an extended period of time, perhaps decades. References Borsa J. 2000. Irradiation of Foods. In: Francis JF, editor.Wiley Encyclopedia of Food Science and Technology. 2nd ed.Vol. 3. New York: John Wiley & Sons. p.1428–1436. Chiasson F, Borsa J, Ouattara B, and Lacroix M. 2004. Radiosensitization of Escherichia coli and Salmonella Typhi in Ground Beef. J Food Protection 67 (6):1157–1162.

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Codex. 2003. Revised Codex General Standard For Irradiated Foods. Codex Stan 106-1983, Rev.1-2003. ftp://ftp.fao.org/codex/standard/en/CXS_106e_1.pdf Egerstrom L. 2004. Midwestern Meat Processors Scramble as Irradiation Firm Liquidates. Knight Ridder Business News, January 15. Hallman GJ. 1998. Efficacy of Methyl Bromide and Cold Storage as Disinfestation Treatments for Guavas Infested with Caribbean Fruit Fly.Tropical Science 38(4):229–232. Hawaii Pride. 2005. www.hawaiipride.com Henson S,Loader R.2001.Barriers to Agricultural Exports from Developing Countries:The Role of Sanitary and Phytosanitary Requirements.World Development (Oxford) 29(1):85–102. IAEA. 2004. Irradiation as a Phytosanitary Treatment of Food and Agricultural Commodities. IAEA-TECDOC-1427. IAEA,Vienna. 181 p. ICGFI. 2005. Clearance Database. www.iaea.org/icgfi/data.htm Kalsec. 2005. Managing Oxidation in Irradiated Meats. http://www.kalsec.com/products/ oxid_irrad_over.cfm Mead PS, Slutsker L, Dietz L, McCaig LS, Bresee JS, Shapiro C, Griffin PM, Tauxe RV. 1999. Emerg Infect Dis 5(5):607–625. Molins RA, Motarjemi Y, Kaferstein FK. 2001. Irradiation: A Critical Control Point In Ensuring The Microbiological Safety Of Raw Foods. Food Control 12(6):347–356. NAPPO. 2003. NAPPO Regional Standards Phytosanitary Measures (RSPM). RSPM No.19. Guidelines for Bilateral Workplans. www.nappo.org/Standards/NEW/RSPM19-e.pdf Olson D. 2004. Food Irradiation Future Still Bright. Food Technology 58(7):112. Osterholm MT, Norgan AP. 2004.The Role of Irradiation in Food Safety. New England J Med 350(18):1898–1901. Sewall AM, Farber JM. 2001. Foodborne Outbreaks in Canada Linked to Produce. J Food Protection 64(11):1863–1877. Stichelbaut F, Herer A. 2004.The Palletron: An X-ray Pallet Irradiator Designed for Food Products. Paper 49H-32. 2004 IFT Annual Meeting, July 12–16, Las Vegas, NV. http:// ift.confex.com/ift/2004/techprogram/paper_24302.htm STOP. 2003. Why Are People Still Dying From Contaminated Food? www.safetables.org/ pdf/STOP_Report.pdf SureBeam. 2001. Fact vs. Fiction: SureBeam Turns The Tide on Irradiated Foods. (Brief Article) Progressive Grocer 80(8):30. Titan Corp. 2001. Press release. March 16. SureBeam IPO priced at $10.00 per share. www.titan.com/investor/archives/pressreleases/2001/010316_surebeam.html TVNZ. 2004. Nuked Mangoes To Hit NZ Shops. TVNZ One News. 20 December. http:// tvnz.co.nz/view/news_national_story_skin/465318%3fformat=html UNDP. 2002. The Vienna Convention and the Montreal Protocol. http://www.undp.org/ seed/eap/montreal/montreal.htm USDA. 1999. Policy on Beef Products Contaminated with E. coli O157:H7. Federal Register: January 19. 64(11):2803–2805. http://www.fsis.usda.gov/OPPDE/rdad/FRPubs/ 97-068N.htm USDA. 2003. Listeria In FSIS Ready-To-Eat Products Shows Significant Decline. http:// www.fsis.usda.gov/OA/news/2003/rtedata.htm USDA. 2004. Microbiological Results of Raw Ground Beef Products Analyzed for Escherichia coli O157:H7. http://www.fsis.usda.gov/Science/2004_EColi_Positive_Results/ index.asp USDA. 2005. FSIS Ground Beef Sampling Shows Substantial E. coli O157:H7 Decline In 2004. http://www.fsis.usda.gov/News_&_Events/NR_022805_01/index.asp World Trade Organization. 2001. Trade and Development. http://www.wto.org/english/ tratop_e/devel_e/devel_e.htm

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 2 ADVANCES IN GAMMA RAY, ELECTRON BEAM,AND X-RAY TECHNOLOGIES FOR FOOD IRRADIATION Marshall R. Cleland, Ph.D.

Introduction Irradiation with ionizing energy is widely used to improve the physical, chemical, and biological properties of materials and commercial products.These diverse applications include curing solvent-free inks, coatings, and adhesives, crosslinking plastic and rubber materials, curing fiberreinforced plastic products, extracting nitrogen and sulfur oxides from combustion gases to reduce acid rain, decomposing toxic compounds in waste water, sterilizing medical devices and pharmaceuticals, and controlling insects and pathogenic organisms in fresh foods. Gamma rays from radioactive nuclides, energetic electrons from particle accelerators, and X-rays emitted by high-energy electron beams are suitable sources of ionizing energy for these applications because they can penetrate substantial thicknesses of solid materials. In comparison, ultraviolet (UV) radiation is used mainly for the treatment of surfaces, thin films, clear water, and air because of its shallow penetration in opaque materials. Typical UV radiation sources cannot provide enough photon energy to produce ionization in most materials. Gamma rays, energetic electrons, and X-rays transfer their energies to materials by ejecting atomic electrons, which can then ionize other atoms in a cascade of collisions.Therefore all of these energy sources can produce similar effects in any irradiated material. The choice of a radiation source for a particular application depends on such practical aspects as thickness and density of the material, dose uniformity ratio, minimum dose, processing rate, and economics. 11

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This chapter describes the characteristics of these ionizing energy sources, their relevant physical properties, methods for generating enough radiation power to meet industrial requirements, and some examples of processing facilities.

Basic Irradiation Concepts Definition and Units of Absorbed Dose The absorbed dose is proportional to the ionizing energy absorbed per unit mass of irradiated material.The effects of the treatment are related to this quantity, which is the most important specification for any irradiation process. The international unit of absorbed dose is the gray (Gy) (McLaughlin and others. 1989). 1 Gy = 1 joule/kilogram (J/kg) 1 Gy = 1 watt-second/kilogram (W-s/kg) 1 kGy = 1 kilojoule/kilogram (kJ/kg) 1 kGy = 1 kilowatt-second/kilogram (kW-s/kg) The obsolete unit of absorbed dose is the rad.This unit is often seen in older papers and is still used in some industries. 1 Gy = 100 rad 10 Gy = 1 krad 100 Gy = 10 krad 1 kGy = 100 krad 10 kGy = 1 Mrad 100 kGy = 10 Mrad Absorbed Dose vs. Emitted Radiation Power The definition of absorbed dose given above can be expressed by the following equation: Da = Fp P T / M

(1)

where Da is the average dose in kilograys (kGy), P is the emitted power of the radiation source in kilowatts (kW),T is the treatment time in seconds (s), and M is the mass of the material in kilograms (kg). Fp is a dimensionless factor that accounts for the fraction of emitted power absorbed by the material. In a typical industrial irradiation process, Fp may be in the range

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13

from 0.25 to 0.50.This power fraction depends on the size and shape of the object and the way it is oriented in the radiation field. Rearranging Equation (1) gives the mass processing rate (ASTM 2002a). M / T = Fp P / Da

(2)

This relationship can be called a unity rule because the processing rate is 1 kg/s with an emitted power of 1 kW, an average dose of 1 kGy, and a power absorption fraction of 1.0. Although these values do not correspond to most industrial processes, the unity rule is easy to remember and it provides a basis for quickly estimating actual processing rates by scaling with the appropriate values of Fp, P, and Da. The dose distribution within an irradiated object is seldom uniform, but it can be determined by Monte Carlo calculations (ASTM 2002b) or by dose mapping (ASTM 2003). For applications where the minimum dose (Dmin) is more important than the average dose Da, Equations (1) and (2) can be modified by replacing Da with Dmin and replacing Fp with fp, a reduced value of the power absorption fraction.The factor fp is based on the simplifying assumption that all parts of the object have received only the minimum dose (Cleland and others. 2002). Temperature Rise vs. Dose The absorption of thermal energy in any material causes a temperature rise according to the following equation: ⌬T = H / c

(3)

where ⌬T is the temperature rise in degrees Celsius (°C), H is the thermal energy absorbed in joules per gram (J/g), and c is the thermal capacity of the material in joules per gram per degree Celsius (J/g/°C). By analogy, the absorption of ionizing energy in any material causes a temperature rise according to the following equation: ⌬T = Da / c

(4)

where ⌬T is the temperature rise in degrees Celsius (°C), Da is the average absorbed dose in kilograys (kGy), and c is the thermal capacity of the material in joules per gram per degree Celsius (J/g/°C). Examples of thermal capacities and temperature rises during irradiation of several common materials are shown in Table 2.1 (Cleland and others. 2003a). Absorbed dose requirements for various industrial irradiation processes

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Table 2.1. Examples of Thermal Capacities in J/g/°C and Temperature Rises in °C/kGy in Several Common Materials Material

Thermal Capacity

Temperature Rise

4.19 2.30 1.05 0.90 0.38

0.24 0.43 0.95 1.11 2.63

Water Polyethylene Polytetrafluoroethylene Aluminum Copper

cover a wide range from 0.1 kGy to 1000 kGy. Most of these processes need less than 100 kGy, while many need less than 10 kGy and some need less than 1 kGy. The temperature rises during irradiation of fresh foods, which have high water contents, are negligible because of the relatively low dose requirements, which seldom exceed a few kilograys. Gamma-Ray Facilities More than 200 gamma-ray facilities are being used for various industrial applications, mainly for sterilizing medical devices and for food irradiation. Gamma rays from cobalt-60 and cesium-137 are allowed by the U.S. Food and Drug Administration and by international standards for food irradiation (CFR 1986; Codex 2003). However, Cs-137 is seldom used because large Cs-137 sources are not readily available.The main commercial suppliers of encapsulated Co-60 sources are located in Canada and the UK (MDS Nordion 2005; PURIDEC 2002). Co-60 is a man-made radionuclide. It can be activated by placing metallic slugs of stable Co-59 in a nuclear power reactor.The absorption of a neutron, which was released by the fission of U-235, changes Co-59 to Co-60. It emits two gamma rays simultaneously with energies of 1.17 and 1.33 million electron volts (MeV). It also emits low-energy beta rays (electrons) with a maximum energy of 0.32 MeV. Co-60 has a half-life of 5.26 years, so the activity decays by 12.35% per year.The total activity in the irradiation facility is replenished by adding new sources every year. Older sources are usually kept in the facility for up to 4 half lives or about 20 years before being replaced. The emitted gamma-ray power from 1 megacurie (MCi) of Co-60 can be calculated as follows: P = 1 x 106 x 3.7 x 1010 x 2.5 x 106 x 1.6 x 10-19

(5)

P = 14.8 x 103 J/s or 14.8 kW

(6)

Gamma Ray, Electron Beam, and X-ray Technologies

Figure 2.1.

15

Photograph of an MDS Nordion Co-60 pencil.

where 1 ⫻ 106 is the source strength in curies, 3.7 ⫻ 1010 is the number of becquerels (Bq) per curie (1 Bq means 1 disintegration per second), 2.5 ⫻ 106 is the combined energy of the two gamma rays in electron volts (eV), and 1.6 ⫻ 10-19 is the conversion factor from electron volts to joules (J).About 9% of the gamma ray power is absorbed internally in an encapsulated Co-60 source, so the emitted power is about 14.8 x 0.91 = 13.5 kW per MCi (Jarrett 1982). Most Co-60 sources are in the form of pencils with a length of 452 mm (17.8 in) and a diameter of 11.1 mm (0.44 in). The nickel-plated cobalt slugs are doubly encapsulated in zircaloy tubes as shown in Figure 2.1 (MDS Nordion 2005).The activity in one pencil can be 14.25 kilocuries (kCi) or 527 terabecquerels (TBq).The pencils are loaded into flat, vertical racks as shown in Figure 2.2.These racks are lowered into deep water-filled pools when personnel need to enter the treatment room. They are raised above the pool water to irradiate product containers passing by the source rack on a conveyor. The treatment room is surrounded by a thick concrete shield, which protects operating personnel from the gamma radiation when the source rack is in the raised position.

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Figure 2.2.

Food Irradiation Research and Technology

Photograph of an MDS Nordion Co-60 source rack.

A drawing of the MDS Nordion Pallet™ irradiator for large pallet loads of low-density packages is shown in Figure 2.3.The power absorption efficiency and the dose uniformity are enhanced by passing product loads at two levels on both sides of the source rack. This design is called a panoramic irradiator.With a source loading of 3 MCi, this type of irradiator can process nearly 30 metric tonnes per hour with a product density

Gamma Ray, Electron Beam, and X-ray Technologies

Figure 2.3.

17

Drawing of an MDS Nordion Pallet™ Co-60 irradiator.

of 0.3 g/cm3 and a minimum dose of 2 kGy. Other types of irradiators may have up to 5 MCi. A drawing of the MDS Nordion Centurion™ gamma-ray facility for treating thinner packages of high-density products is shown in Figure 2.4.The source rack is raised and turned to a horizontal position so that product packages can pass above and below the rack. This conveyor arrangement facilitates automatic transfer of single layers of packages from external pallets to the conveyor before treatment and then back to the original pallets.The tops and bottoms of the packages are presented to the source rack without turning them over. A drawing of the Gray*Star Genesis™ gamma-ray facility, which irradiates products under water, is shown in Figure 2.5.The package containers are closed at the top but open at the bottom.Water is kept out of the containers by injecting air with increasing pressure as they are lowered into the pool.The absorbed dose is determined by the dwell time of the containers, which are placed first on one side and then the other side of the source rack. The rack is never raised above the pool, so there is no need for a concrete shield above ground.This arrangement is called a selfcontained irradiator.The total source loading may be up to 1 MCi of Co60 (Gray*Star 2005). The absorbed dose in materials irradiated with gamma rays decreases exponentially with increasing depth.The tenth value layer (depth to decrease the intensity by a factor of 1/10) in water with a large area rack of Co-60 sources is about 31 cm (Cleland and Pageau 1987).The penetration is inversely proportional to the average material density.With an average

18

Figure 2.4.

Food Irradiation Research and Technology

Drawing of an MDS Nordion Centurion™ Co-60 irradiator.

density of 0.3 grams per cubic centimeter (g/cm3), which might be the highest density for most packages of medical devices, the tenth value layer would be about 1 meter (m).With a product load thickness equal to the tenth value layer, a dose uniformity ratio (DUR = Dmax/Dmin) of about 1.6 could be obtained with treatment from opposite sides.This calculated value for a large area absorber would be increased slightly by edge effects in product loads of finite size.

Gamma Ray, Electron Beam, and X-ray Technologies

Figure 2.5.

19

Drawing of a Gray*Star Genesis™ Co-60 irradiator.

Electron Beam Facilities Accelerated electrons with energies up to 10 MeV are allowed by the U.S. Food and Drug Administration and by the international standards for food irradiation (CFR 1986; Codex 2003).This energy limit was recommended to avoid inducing radioactive nuclides in the food (WHO 1981).The penetration of an electron beam increases in proportion to the electron energy, so it is advantageous to use energies of at least 5 MeV for packages of foods, which may have average densities up to 0.8 g/cm3. Lower elec-

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Food Irradiation Research and Technology

Figure 2.6. Electron beam depth-dose distributions in water, from Monte Carlo calculations.

tron energies can be used for irradiating grains and fluids because their thicknesses can be controlled to match the penetration of the electron beam. The depth-dose distributions in water for electron energies between 5 MeV and 12 MeV are shown in Figure 2.6 (Cleland and others 2003b). Electron penetration in water is nearly the same as in polyethylene because of their similarity in atomic composition (Cleland and others. 2002). For treatment from one side with 10 MeV electrons, the thickness where the exit dose equals the entrance dose is about 3.7 centimeters (cm) (1.5 in), after subtracting the equivalent thicknesses of the electron beam window (40 microns of titanium) and the air space (15 cm) between the window and the water. For treatment from opposite sides with 10 MeV electrons, the thickness can be increased to about 8.6 cm (3.4 in).Then the dose in the middle would be the same as the entrance and exit doses. This thickness is enough to irradiate most retail packages of fresh meat, except for whole turkeys.

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Absorbed Dose vs. Beam Current The absorbed dose in materials irradiated with high-energy electron beams can be expressed by the following equation: D(x) = K(x) Fi I T / A

(7)

where D(x) is the dose in kGy at the depth x, I is the emitted beam current of the electron accelerator in milliamperes (mA),T is the treatment time in minutes (min), and A is the area of the irradiated material in square meters (m2). Fi is a dimensionless factor, which accounts for the fraction of beam current that is intercepted by the material. In practice, this fraction depends on the size and shape of the object and the way it is oriented on the product conveyor. In an industrial process for treating wide flat sheets of material, Fi may be as high as 0.90. K(x) is called the area processing coefficient. It is equal to 6 times the energy deposition per electron per unit area density at the depth x where the dose is specified. Its value can be obtained by Monte Carlo calculations (ASTM 2002a; ASTM 2002b). The surface value of the energy deposition per electron is 1.83 MeV-cm2/g for water irradiated with 10 MeV electrons, so K(0) is 6 x 1.83 = 11.0 kilogray square meter per millampere minute (kGy-mA/ma-min) (Cleland and others. 2003b). Rearranging Equation (7) gives the area processing rate (Cleland and others. 2002;ASTM 2002a). A / T = K(x) Fi I / D(x)

(8)

This relationship can also be called a unity rule because the area processing rate is 1 m2/min with a beam current of 1 mA and a surface dose of 10 kGy (1 Mrad).This rule applies when the product of K(x) and Fi is about 10. Even though these values do not correspond to most industrial processes, this unity rule is easy to remember and provides a basis for quickly estimating actual area processing rates by scaling with the appropriate values of Fi, I, and D(x). Electron Beam Technologies More than 1,000 industrial electron beam (EB) accelerators are now used for a variety of irradiation processes, mainly for treating plastic and rubber products to improve their qualities, and for sterilizing single-use medical devices. Only a few of these machines are being used for food irradiation, but this application is still in its infancy. It now has the advantage

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Food Irradiation Research and Technology

of being based on reliable equipment technologies that have been evolving since the 1950s for other applications. Several different methods are used to produce high-energy, high-power electron beams.These include constant-potential, direct-current systems, microwave linear accelerators (linacs), and radio-frequency, resonant cavity systems (Scharf 1986; Abramyan 1988; Cleland 1992; Cleland and Parks 2003c).The choice of a type of accelerator for a particular application is usually based on the process requirements for electron energy and average beam power. Constant-Potential Accelerators This category includes equipment with maximum electron energies as high as 5 MeV and as low as 0.1 MeV. Accelerators with energies below 0.3 MeV can be used for treating grains and powders and for sterilizing surfaces of packaging materials (Nablo and others 1998; Berejka and others 2004; Morisseau and Malcolm 2004; ESI 2005; AEB 2005; Linac Technologies 2005). Accelerators with higher energies up to 5 MeV are capable of treating retail packages of food.These types of equipment are made in the United States, Japan, France, Russia, and China. Systems in the higher energy range above 0.3 MeV are described briefly below. A simplified diagram of a high-energy, constant-potential accelerator is shown in Figure 2.7. The operation is similar to that of a television picture tube or a computer monitor, except that the voltage is much higher. Low-energy electrons are emitted from a heated cathode connected to the negative terminal of a high-voltage power supply. They are accelerated by the strong electric field in a long, evacuated beam tube that consists of many metallic dynodes separated by glass rings. External highvoltage resistors are connected between the dynodes to establish a uniform electric field along the tube axis.This prevents sparks from occurring inside the tube.After the narrow beam of electrons has been accelerated, it is scanned back and forth along a thin metallic “window” at ground potential. Then the beam emerges into the air to irradiate products on a conveyor. The accelerators in this category use similar acceleration tubes. The main differences are found in the methods used to generate the very high potentials that are needed to irradiate thick materials and products. Most high-voltage, constant-potential generators utilize cascaded rectifier systems to convert alternating current (ac) to direct current (dc) power. However, different methods are used to couple the input ac power to the multiple rectifiers, which are connected in series to produce successively higher dc potentials. There are four basic power coupling methods, which can be classed as

Gamma Ray, Electron Beam, and X-ray Technologies

Figure 2.7.

23

Diagram of a constant-potential, scanned-beam electron accelerator.

inductive or capacitive, series or parallel systems (Abramyan 1988). Insulating Core Transformers™ (ICT) made by Wasik Associates in the USA (Wasik Associates 2005) and Vivirad in France (Vivirad S.A. 2005) are inductive, series-coupled systems. The largest ICTs can provide up to 100 kW of electron beam power at 3 MeV. The Electron TransformerRectifier™ (ELV) accelerators made by the Budker Institute of Nuclear Physics in Russia are inductive, parallel-coupled systems (BINP 2005).The largest ELVs can provide up to 90 kW of electron beam power at 2.5 MeV (Salimov and others 2000). Electron Processing Systems™ (EPS) made by Nissin High Voltage in Japan use capacitive, series-coupled generators. These systems are also called Cockcroft-Walton accelerators, because they have evolved from the primitive accelerator that was used to produce the first man-made nuclear reaction more than 75 years ago.The largest EPS can provide up to 150 kW of electron beam power at 5 MeV (Uehara and others 1993; Nissin Electric Co. 2005). The Dynamitron™ accelerators made by IBA

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Food Irradiation Research and Technology

Figure 2.8. Photograph of an IBA-RDI Dynamitron™ 5 MeV constant-potential electron accelerator.

E-Beam X-Ray Solutions in the USA (Galloway and others 2004; IBA 2005; RDI 2005) and similar equipment made in China (Liang and others 1993) are capacitive, parallel-coupled systems.The largest IBA-RDI Dynamitrons can provide up to 300 kW of electron beam power at 5 MeV. A photograph of this type of accelerator is shown in Figure 2.8.The rectifiers and the acceleration tube are located inside the cylindrical array of coupling electrodes. A drawing of an electron beam processing facility with a 5 MeV Dynamitron is shown in Figure 2.9. Microwave Linear Accelerators Microwave linear accelerators (linacs) can induce high kinetic energies in electron beams without using high-voltage dc generators.The accelerating structure consists of a linear array of many small, evacuated, copper cavities. Strong ac electric fields are generated inside these resonant cavities by injecting high frequency power from a klystron microwave amplifier. Linacs with beam power ratings below 25 kW operate at the S-band frequency, 3000 megahertz (MHz). A few larger

Gamma Ray, Electron Beam, and X-ray Technologies

Figure 2.9. facility.

25

Drawing of an IBA-RDI Dynamitron™ 5 MeV electron beam processing

systems with higher beam power ratings operate at the L-band frequency, 1300 MHz. Low-energy electrons are emitted from a heated cathode at one end of the structure and gain energy while passing through each cavity. Overall energy gains of several MeV per meter can be obtained with a peak power dissipation of several megawatts. The klystron is operated with short, repetitive pulses to avoid overheating the system and to reduce the average electron beam current and power. Linacs are seldom used in the energy range below 5 MeV because they cannot provide as much beam current and power as constant-potential accelerators.Their main advantage is the ability to provide higher electron energies to irradiate thicker products. There are several suppliers of industrial linacs for radiation processing. Mevex Corporation in Canada provides S-band systems in the 5 MeV to 10 MeV range with modest beam power ratings of 5 kW to 10 kW (Mevex Corporation 2005). Linac Technologies S.A. in France provides Circe™ Sband systems with higher beam power ratings up to 20 kW at 10 MeV

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Food Irradiation Research and Technology

Figure 2.10. Photograph of an Iotron Industries Canada IMPELA™ 10 MeV L-band microwave linear electron accelerator (linac).

(Linac Technologies 2005). Titan Scan in the United States provides similar systems (Titan Scan Technologies 2005). Titan has also produced a prototype 5 MeV L-band system with more than 75 kW of beam power. Iotron Industries Canada Inc. offers L-band systems, which can provide 60 kW at 10 MeV. This design was developed by Atomic Energy of Canada Ltd (Hare 1990; Iotron Industries Canada 2005). A photograph of their IMPELA™ linac is shown in Figure 2.10.There are several other linac suppliers in Japan (Kamino 1998), Russia (NIIEFA 2005), and China (Liang and others 1993). Radio-Frequency Accelerators Medium-energy electron beams can be produced by passing the beam once through a single large resonant cavity.These systems operate in the radio frequency (RF) range of about 110 MHz and are energized with triode tubes, which are more efficient than klystrons.The Budker Institute of Nuclear Physics has produced several models of these ILU™ systems

Gamma Ray, Electron Beam, and X-ray Technologies

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Figure 2.11. Illustration of the electron beam paths in a six-pass IBA Rhodotron™ radio-frequency (RF) electron accelerator.

(BINP 2005). Model ILU-8 can provide 20 kW of beam power in the 0.6 MeV to 1.0 MeV range; Model ILU-6M can provide 40 kW of beam power in the 1.0 MeV to 2.0 MeV range; and Model ILU-10 can provide 50 kW of beam power in the 2.5 MeV to 4.0 MeV range (Auslender and Meshkov 1990). Higher electron energies can be produced with a single large resonant cavity by passing the electrons several times through the same cavity. The Rhodotron™ accelerators developed by IBA give an energy gain of 1 MeV per pass. They can achieve up to 10 MeV by passing the beam through a coaxial cavity 10 times (Defrise and others 1995). Lower energies can also be obtained by extracting the beam after fewer passes. An illustration of the beam paths is shown in Figure 2.11.Three Rhodotron models have beam power ratings of 35 kW, 80 kW, and 200 kW at 10 MeV (IBA 2005). A photograph of the lower half of a 200 kW cavity is shown in Figure 2.12. The beam apertures and the beam deflecting magnets can be seen around the middle of the cavity. A more powerful model with six passes has 100 mA of beam current or 500 kW of beam power at 5 MeV

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Food Irradiation Research and Technology

Figure 2.12. Photograph of the lower half of a ten-pass IBA Rhodotron™ RF cavity for a 10 MeV, 200 kW electron accelerator.

and 700 kW at 7 MeV (Abs and others 2004).These high beam power ratings can provide substantial X-ray processing capability, even though the efficiency for X-ray generation is relatively low. The cavity of this accelerator resonates at a frequency of 107.5 MHz. Because of its large diameter (2 meters) and the relatively low energy gain per pass, a Rhodotron cavity can be energized in the continuous wave (CW) mode with an RF power dissipation of about 100 kW. In contrast to a pulsed linac, the electron beam can be scanned rapidly, like a dc beam. This enables the use of high beam power and high conveyor speeds for low-dose applications with high throughput rates. Rhodotron beam scanners can be equipped with special magnets to eliminate beam divergence. This feature gives more uniform dose distributions in packages with different sizes, which have different spacings from the beam window of the accelerator.

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Table 2.2. Comparisons of Basic Properties of Radiation Processing with HighEnergy X-rays at 5 MeV, 7.5 MeV, and 10 MeV in Water Maximum X-Ray Energy (MeV)

X-ray Emission Efficiency (%)

Tenth Value Layer in Water (cm)

Optimum Thickness Two-Sided (cm)

Dose Uniformity Ratio (Dmax/Dmin)

10.0 7.5 5.0 Co-60

16.2 13.3 8.2 Gamma Rays

49.0 44.3 39.0 31.0

43 38 34 28

1.54 1.54 1.54 1.75

X-Ray Facilities X-rays (bremsstrahlung) with energies up to 5 MeV are allowed by the U.S. Food and Drug Administration and by international standards for food irradiation (CFR 1986; Codex 2003). The 5 MeV energy limit was originally approved by the USFDA in response to a petition from RDI (CFR 1964). Later it was recommended by a Joint FAO/IAEA/WHO Expert Committee (WHO 1981). Still later, another IAEA consultant’s meeting recommended increasing the X-ray energy limit to 7.5 MeV (ICGFI 1995; IAEA 2002).This higher value was recently approved by the USFDA in response to a petition from IBA (CFR 2004). X-rays are emitted when energetic electrons strike any material.The efficiency for converting electron beam power to emitted X-ray power increases with the atomic number of the target material and the electron energy. Increasing the energy also improves the X-ray penetration and allows the treatment of thicker packages or heavier products, such as fresh foods.These improvements are indicated by the data given in Table 2.2, which were obtained by Monte Carlo simulations (Meissner and others 2000). Nevertheless the penetration, even with 7.5 MeV X-rays, is still not sufficient to irradiate full pallet loads of fresh foods from opposite sides with acceptable dose uniformity. The Palletron™ system, patented by MDS Nordion and licensed by IBA, provides a solution to this problem (Kotler and Borsa 2003). The drawing in Figure 2.13 illustrates the Palletron concept. Single pallets are irradiated from the side while they are rotating in front of a tall Xray target.When the load density is higher than 0.5 g/cm3, the dose uniformity ratio (DUR) can still be too high because of the X-ray attenuation in the middle of the load. However, the DUR can be improved by placing thick steel collimators on both sides of the scanning X-ray

30

Figure 2.13.

Food Irradiation Research and Technology

Illustration of the Palletron™ rotational X-ray irradiation system.

beam.This reduces the dose near the outside without reducing the minimum dose in the middle of the load.The optimum spacing of the collimators depends on the load density. The treatment of single pallets simplifies the scheduling of products with different densities and different dose requirements. The data presented in Figure 2.14, calculated by Monte Carlo simulation, shows that a DUR below 1.4 can be obtained with product densities up to 0.8 g/cm3, a pallet footprint of 100 cm ⫻ 120 cm, and a pallet height of 180 cm, using either 5 MeV or 7.5 MeV X-rays. The data presented in Figure 2.15, also calculated by Monte Carlo simulation, shows that increasing the maximum X-ray energy from 5 MeV to 7.5 MeV would nearly double the throughput rate with the same electron beam power. The X-ray throughput rate would be about 50 tons per hour with 700 kW of electron beam power at 7.5 MeV, a minimum dose of 2 kGy in the density range from 0.5 g/cm3 to 0.8 g/cm3, and allowing a pallet transfer time of 20 seconds (Stichelbaut and others 2002; Stichelbaut and others 2004).The layout of an X-ray irradiation facility equipped with a Palletron system is shown in Figure 2.16.

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Figure 2.14. Dose uniformity ratio vs. product density with the Palletron™ rotational X-ray irradiator at 5 MeV and 7.5 MeV.

Conclusion Gamma ray, electron beam and X-ray sources are used for a variety of industrial processes. Irradiation of food is a small but growing part of the radiation processing industry. Ongoing developments in radiation sources and processing facilities are increasing their capacity, productivity, and reliability. These mature technologies are able to support a substantial increase in the availability of irradiated food.

Figure 2.15. Hourly throughput rate vs. product density with the Palletron™ rotational X-ray irradiator at 5 MeV and 7.5 MeV.

Figure 2.16.

Layout of a Palletron™ rotational X-ray irradiation facility.

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References Abramyan EA. 1988. Industrial Electron Accelerators and Applications. New York: Hemisphere Publishing Corporation, Harper & Row. 302 p. Abs M, Jongen Y, Poncelet E, Bol J. 2004.The IBA Rhodotron TT1000:A Very High Power EBeam Accelerator. Radiat Phys Chem 71(1-2):287–290. AEB. 2005.Advanced Electron Beams.Web site, www.advancedelectronbeams.com, tel 978 658 8600, mail 10 Upton Drive,Wilmington, MA 01887, USA. ASTM. 2002a. ISO/ASTM 51649:2002(E). Standard Practice for Dosimetry in an Electron Beam Facility for Radiation Processing at Energies Between 300 keV and 25 MeV. Annual Book of ASTM Standards, 12.02,ASTM International, 100 Barr Harbor Drive, PO Box C700,West Conshohocken, Pennsylvania 19428. ASTM. 2002b. ASTM E 2232-02. Standard Guide for Selection and Use of Mathematical Methods for Calculating Absorbed Dose in Radiation Processing Applications. Annual Book of ASTM Standards, 12.02, ASTM International, 100 Barr Harbor Drive, PO Box C700,West Conshohocken, Pennsylvania 19428. ASTM. 2003. ASTM E 2303-03. Standard Guide for Absorbed-Dose Mapping in Radiation Processing Facilities. Annual Book of ASTM Standards, 12.02, ASTM International, 100 Barr Harbor Drive, PO Box C700,West Conshohocken, Pennsylvania 19428. ASTM. 2004. Standards on Dosimetry for Radiation Processing, 2nd Edition, Sept 2004. ASTM International, 100 Barr Harbor Drive, PO Box C700, West Conshohocken, Pennsylvania 19428. 350 p. Auslender VL,Meshkov IN.1990.Powerful Single-Cavity RF Accelerators and Their Use in the Industrial Radiation Chemical Processing Lines. Radiat Phys Chem 35(4-6):627–631. Berejka AJ, Avnery T, Carlson C. 2004. Modular Low-Voltage Electron Beams. Radiat Phys Chem 71(1-2):301–305. BINP. 2005. Budker Institute of Nuclear Physics.Web site, www.inp.nsk.su, tel 383 3 39 47 60, mail Acad. Lavrentiev Prospect 11, 630090 Novosibirsk, Russia. CFR. 1964. Radiation and Radiation Sources Intended for Use in the Production, Processing, and Handling of Food. X-Radiation for Processing Food. Commissioner of Food and Drugs, Department of Health, Education, and Welfare, 21 CFR Part 121 Subpart G, Docket No. 64-13057. Fed Reg, Dec 19, 1964:18056. CFR. 1986. Irradiation in the Production, Processing and Handling of Food, Final Rule. Food and Drug Administration, Department of Health and Human Services, 21 CFR Part 179, Docket No. 81N-0004. Fed Reg 51(75):13376–13399. CFR. 2004. Irradiation in the Production, Processing and Handling of Food, Final Rule. Food and Drug Administration, Department of Health and Human Services, 21 CFR Part 179, Docket No. 2003F-0088. Fed Reg 69(246):76844–76847. Cleland MR, Pageau GM. 1987. Comparisons of X-ray and Gamma Ray Sources for Industrial Irradiation Processes. Nucl Inst Meth Phys Res B24/25:967–972. Cleland, MR. 1992. High Power Electron Accelerators for Industrial Radiation Processing. Chapter 3, In: Eds.A. Singh and J. Silverman. Radiation Processing of Polymers. Munich, Carl Hanser Verlag. New York, Oxford University Press. 23–49. Cleland M, Galloway R, Genin F, Lindholm M. 2002. The Use of Dose and Charge Distributions in Electron Beam Processing. Radiat Phys Chem 63(3-6):729–733. Cleland MR, Parks LA, Cheng S. 2003a. Applications for Radiation Processing of Materials. Proceedings of IRaP 2002, 5th International Symposium on Ionizing Radiation and Polymers. Nucl Inst Meth Phys Res B: Beam Interactions with Materials and Atoms 208:66–73.

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Cleland MR, Lisanti TR, Galloway RA. 2003b. Equations Relating Theoretical Electron Range Values to Incident Electron Energies for Water and Polystyrene. RDI-IBA TIS 1556. IBA E-Beam X-Ray Solutions, 151 Heartland Blvd, Edgewood, New York 11717. Cleland MR, Parks LA. 2003c. Medium and High-Energy Electron Beam Radiation Processing Equipment for Commercial Applications. Proceedings of IRaP 2002, 5th International Symposium on Ionizing Radiation and Polymers. Nucl Inst Meth Phys Res B: Beam Interactions with Materials and Atoms 208:74–89. Codex. 2003. Codex General Standard for Irradiated Foods (CODEX STAN 106-1983, Rev. 1-2003. 2 p.) and Recommended International Code of Practice for the Radiation Processing of Food (CAC/RCP 19-1979, Rev. 2-2003. 7 p.). Codex Alimentarius Commission, Food and Agriculture Organization and World Health Organization,Viale delle Terme di Caracalla, 00100 Rome, Italy. Defrise D,Abs M, Genin F, Jongen Y. 1995.Technical Status of the First Industrial Unit of the 10 MeV, 100 kW Rhodotron. Radiat Phys Chem 46(4-6):473–476. ESI. 2005. Energy Sciences Inc. Web site, www.ebeam.com, tel 978 694 9000, mail 42 Industrial Way,Wilmington, MA 01887, USA. Galloway RA, Lisanti TR, Cleland MR. 2004.A New 5 MeV-300 kW Dynamitron for Radiation Processing. Radiat Phys Chem 71(1-2): 551–553. Gray*Star. 2005. web site, www.graystarinc.com, tel 973 398 3331, mail 200 Valley Road, Suite 103, Mt.Arlington, NJ 07856, U.S.A. Hare GE. 1990. IMPELA Electron Accelerators for Industrial Radiation Processing. Radiat Phys Chem 35(4-6):619–626. IAEA. 2002. Natural and Induced Radioactivity in Food. IAEA-TECDOC-1287, ISSN 10114289, International Atomic Energy Agency, Wagramer Strasse 5, PO Box 100, A-1400 Vienna,Austria. 136 p. IBA 2005. Web site, www.iba-worldwide.com, tel 32 10 47 58 92, mail Chemin du Cyclotron 3, 1348 Louvain-la-Neuve, Belgium. ICGFI. 1995. The Development of X-Ray Machines for Food Irradiation. Proceedings of a Consultant’s Meeting, Oct 16–18, 1995. International Consultative Group on Food Irradiation (ICGFI), International Atomic Energy Agency, Wagramer Strasse 5, P.O. Box 100,A-1400 Vienna,Austria. 17 p. Iotron Industries Canada Inc. 2005.Web site, www.iotron.com, tel 604 945 8838, mail 1425 Kebet Way, Port Coquitlam, British Columbia, Canada V3C 6L3. Jarrett RD, Sr. 1982. Isotope (Gamma) Radiation Sources. Chapter 6, In: Eds, E.S. Josephson and M.S. Peterson. Preservation of Food by Ionizing Radiation,Vol. I. Boca Raton, Florida 33431: CRC Press. 137–163. Kamino Y.1998.10 MeV 25 kW Industrial Electron Linac.Radiat Phys Chem 52(1-6):469–473. Kotler J, Borsa J. 2003; MDS Nordion, assigned to MDS (Canada) Inc., Kanata, Canada. Product Irradiator for Optimizing Dose Uniformity in Products. Patent Descriptor, United States Patent No. US 6,504,898 B1. Date issued, January 7, 2003. Liang X, Qian J, Zhai X, Wang D, Zhu X. 1993. Development and Application of Electron Accelerators for Radiation Processing in China. Radiat Phys Chem 42(1-3):519–523. Linac Technologies S.A. 2005.Web site, www.linactechnologies.com, tel 33 1 69 35 24 00, mail 16 rue Nicolas Appert, 91400 Orsay, France. McLaughlin WL, Boyd AW, Chadwick KH, McDonald JC, Miller A. 1989. Dosimetry for Radiation Processing. New York, NY:Taylor and Francis. 251 p. MDS Nordion. 2005. Web site, www.mds.nordion.com, tel 613 592 2790, mail 447 March Road, Ottawa, ON K2K 1X8, Canada. Meissner J,Abs M, Cleland MR, Herer AS, Jongen Y, Kuntz F, Strasser A. 2000. X-Ray Treatment at 5 MeV and Above. Radiat Phys Chem 57(3-6):647–651.

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Mevex Corporation. 2005. Web site, www.mevex.com, tel 613 831 2664, mail 108 Willowlea Road, P.O. Box 1778, West Carleton Industrial Park, Stittsville, Ontario, K2S 1B4, Canada. Morisseau D, Malcolm F. 2004. SterStar System: Continuous Sterile Transfer by E-Beam. Radiat Phys Chem 71(1-2):555–558. Nablo SV, Wood JC, Jr, Desrosiers MF, Nagy VY. 1998. A Fluidized Bed Process for Electron Sterilization of Powders. Radiat Phys Chem 52(1-6):479–485. NIIEFA. 2005.The D.V. Efremov Scientific Research Institute of Electrophysical Apparatus. Web site, www.niiefa.spb.su, mail 3 Doroga na Metallostroy, Promzona “Metallostroy”, St. Petersburg 196641, Russia. Nissin Electric Co. 2005. Web site, www.nissin.co.jp, tel 81 75 864 8849, mail 47 UmezuTakase-cho, Ukyo-ku, Kyoto 615-8686, Japan. PURIDEC Irradiation Technologies. 2002.Web site, www.puridec.co.uk, tel 44 1494 77444, mail 6 Chiltern Court,Asheridge Road, CHESHAM, Buckinghamshire, England HP5 2PX. RDI. 2005. Radiation Dynamics Inc.Web site, www.e-beam-rdi.com, tel 631 254 6800, mail 151 Heartland Boulevard, Edgewood, New York 11717, U.S.A. Salimov RA, Cherepkov VG, Golubenko JI, Krainov GS, Korabelnikov BM, Kuznetsov SA, Kuksanov NK, Malinin AB, Nemytov PI, Petrov SE, Prudnikov VV, Fadeev SN, Veis ME. 2000. D.C. High Power Electron Accelerators of ELV-Series: Status, Development, Applications. Radiat Phys Chem 57(3-6):661–665. Scharf,Waldemar. 1986. Particle Accelerators and Their Uses, Part 1 Accelerator Design, Part 2 Applications of Accelerators, New York, NY: Harwood Academic Publishers. 1050 p. Stichelbaut F, Bol J, Cleland MR, Gregoire O, Herer AS, Jongen Y, Mullier B, Rose G, Vander Donckt M. 2002. The Palletron: A High Dose Uniformity Pallet Irradiator with X-Rays. American Institute of Physics (AIP) Conference Proceedings 680:891–894. Stichelbaut F, Bol J, Cleland MR, Gregoire O, Herer AS, Jongen Y, Mullier B. 2004. The Palletron:A High-Dose Uniformity Pallet Irradiator with X-Rays. Radiat Phys Chem 71(12):291–295. Titan Scan Technologies. 2005.Web site, www.titanscan.com, tel 858 812 6500, mail 9020 Activity Road, Suite D, San Diego, CA 92126, U.S.A. Uehara S,Taniguchi S, Kashiwagi M, Mizusawa K, Sakamoto I, Hoshi Y,Tomita K. 1993.A 5 MV 30 mA EB/X-Ray Processing System. Radiat Phys Chem 42(1-3):515–518. Vivirad S.A. 2005.Web site, www.vivirad.com, tel 33 3 88 69 13 25, mail 23 Rue Principale, 67117 Handschuheim (Strasbourg), France. Wasik Associates. 2005. Web site, www.wasik.com, tel 978-454-9787, mail 29 Diana Lane, Dracut, MA 01826, U.S.A. WHO. 1981.Wholesomeness of Irradiated Food. Report of a Joint FAO/IAEA/WHO Expert Committee, World Health Organization, Technical Report Series 659, Geneva, Switzerland. 33 p.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 3 REGULATION OF IRRADIATED FOODS AND PACKAGING George H. Pauli, Ph.D.

Introduction I would like to take this opportunity to discuss the process that FDA follows in the regulation of irradiated foods and irradiated food packaging. I have found that people who have not been intimately involved in the process often assume what is required and therefore may not understand the reasons for FDA actions.An overview of FDA’s activities prior to 1986 has been previously published (Pauli and Takeguchi, 1986). First, FDA’s premarket approval authority for irradiated foods and packaging derives from the Food Additives Amendment of 1958. In that legislation, the definition of a food additive reads, in part, as follows: Any substance the intended use of which results or may reasonably be expected to result, directly or indirectly, in its becoming a component or otherwise affecting the characteristics of any food (including any substance intended for use in producing, manufacturing, packing, processing, preparing, treating, packaging, transporting, or holding food; including any source of radiation intended for any such use) . . . (emphasis added). Although there are exceptions to this definition, use of a source of radiation to treat food always requires approval. Section 402(a)(7) of the Federal Food, Drug, and Cosmetic Act reads: A food shall be deemed to be adulterated—if it has been intentionally subject to radiation, unless the use of radiation was in conformity with a regulation or exemption pursuant to section 409. 37

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Section 409 provides the general safety and procedural rules for approving use of all food additives, including a source of radiation. Approving regulations may be promulgated by proposal and comment rulemaking initiated by FDA, or by a petition submitted by an interested party that is announced by a filing notice and decided upon by a final regulation. Generally, petitions are the more efficient route to a regulation because: (1) they focus on specific applications of sufficient interest to someone to cause them to prepare documentation of safety; and (2) because FDA can simply publish a notice of filing rather than a proposed rule describing the basis for issuing a regulation and solicitation of comments. Although FDA considers comments addressed to a petitioned action announced in a notice of filing, and although this may complicate the effort, it is less labor intensive to FDA than the proposal route. Importantly, a petition places an action on FDA’s agenda whereas many competing goals are considered before FDA decides to issue a proposal. As of July 2004, FDA had eight active petitions on its agenda. The subjects of the petitions and the petitioners are as follows: Subject

Petitioner

Reduce microorganisms on fresh or frozen molluscan shellfish

National Fisheries Institute and Louisiana Dept. of Agriculture and Forestry USDA/FSIS

Control microorganisms on non-chilled meat food products (“hot-boned” meat) Raise dose and change packaging requirements for poultry Control pathogens in multiple ingredient foods Control pathogens in crustaceans Control microbial contamination on dietary supplements Use of X-rays generated from machine sources at energies not to exceed 7.5 MeV1 Use of sterilizing doses for shelf stable foods

USDA/FSIS Food Irradiation Coalition/NFPA National Fisheries Institute Steris Corporation IBA (Now Sterigenics International, Inc.) IBA (Now Sterigenics International, Inc.)

Most of these petitions have been with FDA for a considerable time. This is disappointing because FDA places a priority on food additive petitions intended to provide technology for controlling pathogens. Because FDA considers the status of a petition to be confidential until a decision is reached (except for communication with the petitioner to

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resolve important issues), the absence of information can lead to unwarranted speculation. Because of the long time, and because some of the reason for delay is now public information, I thought it would be helpful to discuss the essence of a petition review in the context of the petition from the Food Irradiation Coalition/NFPA. The first thing we do when we receive a petition is to determine the scope of the petition. Specifically, we try to determine what the regulation would say if we approved the petition.Although this determination is fundamental, it is often more difficult than it seems, because a petitioner may know what it wants to have approved, but putting it into words may go far beyond the petitioner’s intent and may raise difficult issues in which it has little or no interest. An approving regulation is generic—applicable to everyone, not just the petitioner. Therefore, the petitioner’s intent is not as important as what a regulation would allow. After the scope is known, we look to see whether there could be any safety questions that had not been directly and completely addressed by previous decisions. This may result from new information or expanded scope. We look to see how the petitioner has addressed such issues. We ask whether anything else in the published literature or FDA files may be relevant to such issues. Finally, we determine whether any comments have been submitted to the Docket for the petition and, if so, we evaluate whether the comments have met the burden for supporting the action they request, just as we evaluate whether the petitioner has met the burden of safety demonstration with its petition. I will now use the petition mentioned above to discuss how this is done. The petition, received in 1999, is quite broad in scope. We exchanged correspondence with the petitioner several times to clarify what all would be covered.After publishing a notice of filing, in general terms, we discovered that our notice was too narrow and published a second, amended notice to ensure that the public had been notified of everything under consideration. Previous decisions by FDA on irradiated foods had generally been for raw agricultural commodities or single-ingredient foods.This petition addressed previously processed foods that would have the variety of ingredients we see on an ingredient list.Also, previous decisions pertained to foods containing minimal amounts of carbohydrate, except for those foods that were irradiated only at a very low dose, or that were an insignificant amount in the diet.Thus, we needed to address the question of the effects of irradiation on common food ingredients as well as the effect on carbohydrates. Our chemistry reviewer examined published literature on irradiation of high-carbohydrate foods (Diehl, 1982). Among other things, he found a reference to an unpublished report of furan in ir-

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radiated apple juice but not in heat-processed juice (Dubois and others, 1966).After obtaining a copy of the report, he concluded that the identification of furan was neither well supported nor quantified. However, because furan was listed on the U.S. Department of Health and Human Services 8th Report On Carcinogens in 1998 and remains listed today in the 11th Report (USHHS, 2005), we concluded that we had to understand the consequence of this finding more completely. To follow up on this report, our chemist irradiated apple juice and verified that the authors were correct; low levels of furan were produced when apple juice was irradiated (Morehouse, 2001).To obtain more information, FDA began a collaborative effort with the petitioner to determine whether furan was limited to fruit juice or whether there were broader ramifications. Reports were identified with non-quantified amounts of furan in heat-processed, but not irradiated, foods.Thus, we extended the effort to look at other processed foods. In sum, we discovered that furan appears to occur more commonly in foods than previously thought. Importantly, it appears to be formed through a variety of mechanisms from several precursors.Three mechanisms that have been elucidated include thermal degradation of carbohydrates, thermal oxidation of lipids, and decomposition of ascorbic acid or its derivatives (FDA, 2004). Levels found in heat-processed foods purchased in the supermarket generally contained higher levels than those found in irradiated foods2 (FDA,2004).FDA announced these findings on May 10, 2004, with a call for data on the occurrence of furan in foods, mechanisms of furan formation, and mechanisms of furan toxicity, and discussed their significance at a Food Advisory Committee meeting on June 8, 2004. Information on this issue is posted on FDA’s Web site at http://www.cfsan.fda.gov/~lrd/pestadd.html.We continue to evaluate the significance of furan. Because of the focus on foods currently on the market, the research on irradiated foods has not been completed sufficiently at this time for publication. I mentioned earlier that we also evaluate comments received. Because we have not reached a final decision, I cannot discuss what our decision will be.The comments are public, however and, as of July 2004, generally fall into the following six categories: (1) the commenters disagree with specific conclusions in a 1999 book on high dose food irradiation issued by the World Health Organization; (2) the commenters express concern about 2-alkylcyclobutanones produced when fat is irradiated; (3) the commenters believe irradiation will increase the levels of trans-fats; (4) the commenters were concerned with reports of polyploidy reported in India in the 1970s; (5) the commenters were concerned with the ratio of reports of mutagenicity compared to those that report no mutagenicity; (6) the commenters believe that more research is needed.

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It is also worth noting that although FDA’s decisions on irradiated food become effective when published, those who believe that FDA erred may file objections within 30 days of a decision and request an evidentiary hearing. FDA has received objections to its decisions on irradiated eggs, irradiated seeds, and radiation systems used to inspect cargo. Finally, as with all its food additive approvals, FDA decisions are based on conditions of use.When FDA reviews the safety of packaging, it considers the type of food in the package (dry, aqueous, oily) and the temperature permitted for food contact. FDA considers that irradiating a package with food inside is a condition that needs explicit review. Although various approvals were issued several decades ago, there has been little in the approval agenda in recent years. FDA is now authorized to evaluate safety via a 120-day notification process, making the petition process for packaging a remnant of the past.At present, FDA has no effective notifications for irradiated packaging. FDA has been working on guidance in this area but nothing has been issued.

Notes 1.This petition was approved on December 23, 2004. 2. Importantly, although quantifiable amounts have been identified in heat-processed foods, irradiated foods currently on the market (which have not been heat-processed) do not appear to contain sufficient furan to be quantified (limit of quantitation is 2–5 ppb depending of the food type).

References Pauli, G.H., and Takeguchi, C. A. 1986. Irradiation of Foods - An FDA Perspective, Food Reviews International,Vol. 2, 79–107. Diehl, J.F. 1982. Radiolytic Effects in Foods, in Preservation of Food by Ionizing Radiation, Edward S. Josephson and Martin S. Peterson, ed. CRC Press, Inc., Boca Raton, Florida Dubois, P., Zenz, H. Stehlic, G., and Kaindl, 1966.Analysis of the volatile components in irradiated apple and grape juices, Seibersdorf Project Report SPR-8. U.S. Department of Health and Human Services, 11th Report On Carcinogens, (2005) http://ntp.niehs.nih.gov/index.cfm?objectid=32BA9724-F1F6-975E-7FCE50709CB4C932. Morehouse, K., Personal communication (2001) Transcript of June 8, 2004 FAC meeting at: http://www.fda.gov/ohrms/dockets/ac/04/transcripts/204-4045t2b-02.htm Exploratory Data on Furan in Food, FDA. 2004. (updated 2005) http://www.cfsan.fda.gov/ ~dms/furandat.html.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 4 TOXICOLOGICAL SAFETY OF IRRADIATED FOODS Christopher H. Sommers, Henry Delincée, J. Scott Smith, and Eric Marchioni

Introduction Generation of cancers in animals requires the mutation or deletion of oncogenes or tumor suppressor genes, resulting in a loss of heterozygosity at those allele locations. Mutation (point mutations or frame-shift mutations) and deletion of genes can be induced by exposure of cells to genotoxic chemicals or can occur naturally as part of the cellular DNA repair and replication process (Ames and Gold 1990). Many consumers are simply unaware that foods contain carcinogens, either natural or artificial, and cause cancer. A very small subset of naturally occurring carcinogens in foods include compounds such as benzene and formaldehyde (Smith and Pillai 2004; Fan and Thayer 2002). A number of studies have confirmed the mutagenicity of cooked meats and their fats, and the formation of nitrosamines as part of the meat curing and cooking process (Knekt and others 1999).Tumor promoters present in cooked meat and poultry include oxidization products of fats and oils, heme, and cholesterol (Van der Meer-van Kraaij and others 2005; Yang and others 1998; Tseng 1996).Alcohol is known to induce the formation of tumors in the gastrointestinal tract of rodents (Mufti 1998). It was recently found that high-temperature frying and baking of starch-containing foods results in the formation of acrylamide, a suspected human carcinogen (Friedman 2003). Furan, a carcinogen in animals, is formed in foods as a result of thermal processing (Perez-Locas and Yaylayan 2004). Compounds used in the pickling, salting, and smoking processes are associated with gastro-intestinal cancers in humans (Weisburger and Jones 1990). Discussions pertaining to food irradiation 43

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therefore have to be placed in context with the risks associated with consumption of irradiated foods versus foods processed using technologies and additives that are known to cause cancer in animals and humans.

Food Irradiation Food irradiation is perhaps the single most studied food processing technology for toxicological safety in the history of food preservation. Studies pertaining to the safety and nutritional adequacy of irradiated foods date back to the 1950s and were frequently associated with the use of radiation to sterilize foods. Hundreds of short-term and long-term safety studies led to the approval of one or more foods for irradiation by presently more than sixty countries.These studies are thoroughly reviewed in The Safety and Nutritional Adequacy of Irradiated Foods, published by the World Health Organization (WHO 1994). In the United States, the Food and Drug Administration reviewed the available studies for the quality of experimental design, rigor, and statistical validity before approving irradiation of a variety of food products including grain, fruits and vegetables, spices and dried herbs, meat and poultry, and eggs for human consumption (Federal Register 2005; WHO 1994).The vast majority of the studies failed to find adverse effects associated with consumption of or exposure to irradiated foods. Not surprisingly, a small number of studies produced equivocal results pertaining to the safety of irradiated foods. However, in-depth review of those studies determined that they were deficient in experimental design, used insufficient numbers of test subjects for proper statistical analysis, or suffered from experimenter error (WHO 1994). The preferred method for assessing the toxicological safety of irradiated foods has been long-term feeding studies in animals, often for multiple generations. Toxicologists prefer to use animals for these types of evaluations, as opposed to using people or their children, for obvious reasons. Swallow (1991) reported that animals used for toxicological research, fed diets of radiation-sterilized foods for 40 generations, suffered no ill effects from consumption of irradiated foods. Thayer and others (1987) reported that rodents fed diets of radiation-sterilized chicken meat (45–68 kGy) did not suffer an increased risk of cancer or birth defects. The same study also failed to find adverse affects associated with long-term consumption of irradiated meat in beagle dogs. De Knechtvan Eekelen and others (1971, 1972) conducted single- and multiplegeneration feeding studies in rats without finding adverse effects due to consumption of the irradiated chicken diet. Poling and others (1955) re-

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ported no evidence of changes in survival, histopathology, or reproduction in three generations of rats fed radiation-sterilized ground beef. Feeding studies in animals have been very consistent in the lack of adverse effects associated with long-term consumption of irradiated foods.

Benzene, Formaldehyde and Amines The presence of several compounds, most notably benzene and toluene, has generated some concerns about the safety of irradiated foods. It was originally thought that trace amounts of benzene were formed in irradiated foods and that this was a unique situation. It is currently thought that benzene and toluene are produced from the oxidative/radiolytic cleavage of phenylalanine.They have been reported in irradiated beef (Merritt and others 1978; Nam and others 2003), though in the 5–60 ppb range. Benzene and its derivatives are not typically found in raw food products, but it appears that thermal treatments do produce trace amounts in some cooked products. Matiella and Hsieh (1991) identified benzene derivatives in scrambled eggs, whereas McNeal and others (1993) reported the presence of benzene in butter, eggs, meat, and certain fruits with levels ranging from 0.5 ppb in butter to 500–1900 ppb in eggs.Angelini and others (1975) evaluated volatile compounds in fresh and irradiated haddock and found benzene and toluene in all samples with larger quantities present in the irradiated ones. In 1979 the Federation of American Societies for Experimental Biology evaluated 65 compounds found in irradiated beef and noted that small amounts of benzene could be detected in both irradiated (56 kGy) and untreated beef (Chinn 1979a). Gamma and electron-irradiated beef contained about 18–19 ppb, which was reduced to 15 ppb upon cooking. On the other hand, the thermally-sterilized and frozen controls contained no detectable benzene, but on cooking the levels were approximately 2–3 ppb.They concluded that such small amounts of benzene did not constitute a significant risk. Health Canada (Bureau of Chemical Safety), in a recent evaluation (2002) of an application for irradiated ground beef, has estimated that approximately 3 ppb of benzene would be formed in irradiated beef at the typical dose ranges (1.5–4.5 kGy) and concluded that it is of insignificant health risk. Formaldehyde and malonaldehyde are probably formed in most foods containing carbohydrates (Dauphin and Saint Lebe 1977). Usually the formed formaldehyde is very reactive and will readily form covalent links with proteins and other constituents.Thus, unless the food item is low in

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protein or contains a considerable amount of water, it would not be present. Fan (2003) has shown that formaldehyde can be generated from solutions of fructose, glucose, and sucrose. Significant amounts were also observed in both pasteurized and fresh irradiated apple juice (Fan and Thayer 2002). Lee and others (1973) observed slight increases in formaldehyde amounts in irradiated Irish Cobbler potatoes at doses of 1.5 kGy. Irradiation has been suggested as a way to control nitrosamine formation in cured meat products such as bacon (Fiddler and others 1985). Ahn and others (2004), using water solutions, have shown that the nitrosamines, nitrosodimethylamine, and nitrosopyrrolidine were significantly reduced by gamma irradiation in addition to residual nitrite levels. However, the reduction was not apparent unless the irradiation dose was 10 kGy or higher, an unrealistically high dose. Similar results were observed when using irradiated cooked pork sausage where doses of 5 or 10 kGy reduced residual nitrite levels and nitrosodimethylamine and nitrosopyrrolidine (Ahn 2004).Thus it appears that irradiation can destroy preformed nitrosamines directly or, by limiting residual nitrite or reactive nitrogen compounds, can inhibit the formation upon cooking. Use of irradiation to reduce other toxic nitrogenous compounds, the biogenic amines, has been evaluated in fermented soybean paste. Irradiation of the paste prior to fermentation did not produce any differences compared to controls.After fermentation for 12 weeks, there were significantly lower amounts of histamine, putrescine, tryptamine, and spermidine in the treated samples, suggesting that irradiation may have altered the microflora to one not conducive to biogenic amine formation (Kim and others 2003). Levels of the biogenic amines putrescine, tryptamine, spermine, and spermidine were reduced in pepperoni subjected to gamma irradiation (5–20 kGy) prior to storage (4° C, 4 wk), again suggesting reduction in bacterial numbers (Kim and others 2005).

Formation and Levels of 2-ACBs in Foods Particular attention has been drawn to a special class of cyclic compounds being formed on irradiation of lipids.A wealth of radiolytic products are formed on irradiation of, for example, triglycerides, among them fatty acids, hydrocarbons, aldehydes, ketones, esters, and dimeric and polymeric components (Nawar 1978, 1986; Stewart 2001), but to date one class of components, the 2-alkylcyclobutanones (2-ACBs), is of particular interest. This new class of cyclic components was reported more than 30 years ago (LeTellier and Nawar 1972) to be formed on irradiation

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Figure 4.1. Formation of 2-ACB on irradiation of a triglyceride (LeTellier and Nawar 1972; Nawar 1978, 1986; see also Stewart 2001).

of pure saturated triglycerides containing C6, C8, C10, C12, C14, C16, and C18 fatty acids with a high dose (60 kGy under vacuum). These compounds were identified as the 2-alkylcyclobutanones of the same carbon number as the precursor fatty acid. It has been proposed that these compounds may result from cleavage of the acyl-oxy bond via the formation of a six-membered ring intermediate (Figure 4.1). 2-Dodecylcyclobutanone (2-dDCB) derived from palmitic acid (C16) was also identified in an irradiated synthetic phospholipid, that is, dipalmitoyl-phosphatidyl-ethanolamine, which had been treated with a very high radiation dose (500 kGy under air) (Handel and Nawar 1981). It was, however, not before 1990 that a 2-ACB was identified in irradiated food. Stevenson and others (1990) reported the detection of 2-dDCB in chicken irradiated at a dose of 5 kGy. Subsequent work indicated that the 2-ACBs are radiation specific because they are not detected in raw, cooked, frozen, freeze-dried, spoiled chicken, thermally sterilized chicken stored at room temperature for 12–13 years, or chicken exposed to modified atmospheres (Boyd and others 1991; Crone and others 1992a, b; Stevenson and others 1993). In another approach Ndiaye and others (1999a) treated an aqueous suspension of a synthetic mixture of pure saturated triglycerides (C10, C12, C14, C16 and C18) with microwaves (20 min at 750 W, 2450 MHz),

48 Table 4.1.

Food Irradiation Research and Technology Radiation-Induced Formation of 2-ACBs from Their Precursor Fatty Acids

Fatty Acid

2-alkylcyclobutanone

C 10:0

Capric acid

C 12:0

Lauric acid

C 14:0

Myristic acid

C 16:0

Palmitic acid

C 16:1

Palmitoleic acid

C 18:0

Stearic acid

C 18:1

Oleic acid

C 18:2

Linoleic acid

C 18:2

Linolenic acid

2-hexyl-cyclobutanone (2-HCB) 2-octyl-cyclobutanone (2-OCB) 2-decyl-cyclobutanone (2-DCB) 2-dodecyl-cyclobutanone (2-dDCB) 2-(dodec-5⬘-enyl)-cyclobutanone (2-dDeCB) 2-tetradecyl-cyclobutanone (2-tDCB) 2-(tetradec-5⬘-enyl)-cyclobutanone (2-tDeCB) 2-(tetradeca-5⬘,8⬘-dienyl)-cyclobutanone (2-tD2eCB) 2-(tetradeca-5⬘,8⬘,11⬘-trienyl)-cyclobutanone (2-tD3eCB)

with heat in a convection oven (30 min at 150° C), with UV irradiation (60 min with ␭ 240–280 nm), with high pressure (60 min with 6000 bar) and with ultrasound (5 min at 455 W, 20 kHz) and were unable to detect any 2-ACBs. However, if the triglyceride solution was irradiated, all the corresponding 2-ACBs could be identified.Thus every fatty acid gives rise to its own 2-ACB (Table 4.1). To date, 2-ACBs have not been identified in nonirradiated foods.An exotic occurrence may be the possible presence of 2-methylcyclobutanone in Hevea brasiliensis (Nishimura and others 1977).These authors speculated that the cyclization of isoprene components after sonication could lead to the cyclobutanone structure, but as mentioned previously, when saturated triglycerides were treated with sonication, no 2-ACBs could be detected (Ndiaye and others 1999a).This seems to support the hypothesis that 2-ACBs may be radiation specific, thus being “Unique Radiolytic Products.” However, the possibility also exists that available detection methods of 2-ACBs are just not sensitive enough, so the amount possibly present also in non-irradiated foods is at the moment below the detection limit of the analytical methods (Ndiaye and others 1999a). The occurrence of 2-ACBs in many irradiated foodstuffs has now been confirmed in meat (beef, pork, lamb), poultry (chicken, mechanically re-

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covered poultry meat), liquid whole egg, cheese (Camembert, Brie, or cheese made from sheep’s milk), seafood (prawns), fish (sardine, trout, salmon), fruit (mango, papaya, avocado), nut (peanut), seeds (perilla), and cereals (rice) (see references in EN 1785:2003). 2-dDCB could be also identified in foods irradiated at very low doses (0.05–0.1 kGy) such as onions, garlic, rice, or cowpeas (Horvatovich and others 2002a; Ndiaye 1998; Ndiaye and others 1999b). The levels of 2-ACBs seem to vary in different foods. Of course, this depends on the fat content of the food, its fatty acid composition, and the dose of radiation. Also, the irradiation temperature plays a role, less 2ACBs being formed in frozen foodstuffs. Generally a linear dose dependency of the formation of 2-ACBs has been observed (Stevenson 1992, 1994; Stevenson and others 1993; Crone and others 1992a, b; Ndiaye and others 1999a; Stewart and others 2000; Park and others 2001;Tanabe and others 2001; Gadgil and others 2002; Burnouf and others 2002). Mostly, the level of 2-ACBs is given per gram of fat and is reflective of the fatty acid composition of the meat. For chicken meat, values between 0.15 and 0.75 μg 2-dDCB / g lipid / kGy have been reported (Stevenson and others 1992, 1993, 1996; Boyd and others 1991; Crone and others 1992a, b, 1993; Meier and others 1996; Stewart and others 2001;Tanabe and others 2001), whereas values for 2-tDCB were about 0.05–0.1 μg / g lipid / kGy.The levels in pork meat varied from 0.13–0.21 μg 2-dDCB / g lipid / kGy and 0.12–0.27 μg 2-tDCB / g lipid / kGy (Stevenson 1994, 1996; Stewart and others 2001; Park and others 2001). For beef the reported 2-dDCB yield was about 0.1–0.18 μg / g lipid / kGy, and for 2-tDCB it amounted to be ~ 0.14 μg / g lipid / kGy (Stevenson 1994; Gadgil and others 2002). A systematic approach was taken by Ndiaye and others (1999a), who related the amount of 2-ACBs to the precursor fatty acid. For several foodstuffs (cheese, sardine, trout, beef, and poultry meat) irradiated between 0.1 and 3.1 kGy, the yield of saturated 2-ACBs was reported to be between 1.0 and 1.6, in average 1.3 ± 0.2 nmol / mmol precursor fatty acid / kGy.This indicated that the amount of 2-ACBs (in this case, saturated 2ACBs) formed is relatively independent of the food or food matrix and mostly reflects the amount of precursor fatty acid.This was confirmed by Burnouf and others (2002), who irradiated various types of foods, that is, milk powder, hazelnuts, chicken, beef, goose liver, cocoa, ground beef patties, smoked salmon, frog legs, chicken quenelles, salmon, avocado, liquid whole egg, and noticed that in general similar yields expressed in nmol 2-ACBs / mmol precursor fatty acid / kGy were obtained, although some variation was obvious.This variation could possibly be ascribed to different positions of the fatty acids in the triglycerides (Stevenson 1994). In a

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recent study Horvatovich and others (2005) reported that the formation of saturated 2-ACBs (2-dDCB, 2-tDCB) in chicken, liquid whole egg, and avocado was 1.4 ± 0.4 nmol / mmol precursor fatty acid / kGy. For the formation of mono-unsaturated 2-ACBs (cis-2-dDeCB, cis-2-tDeCB) from the same foods, a slightly lower value of 0.9 ± 0.3 nmol / mmol precursor fatty acid / kGy was found, although this value was found not to be significantly different from the value for the saturated 2-ACBs (Horvatovich and others 2005). In a study with pure triacylglycerides (C16, C18, C18:1, C18:2, C18:3) and the corresponding authentic fatty acids, different radioproduction yields were reported (Kim and others 2004), with the highest levels of 2-ACBs being observed for the saturated triglycerides. In food with mixed triglycerides and usually low amounts of free fatty acids, phospholipids, sterols and other fat components, the radioproduction levels seem to vary only slightly (Ndiaye and others 1999a; Burnouf and others 2002; Horvatovich and others 2005).Therefore, if the fat composition of the food sample is known, the levels of 2-ACBs can be roughly predicted. Considering the edible fat containing only triglycerides and restricting this rough calculation only to the four most common fatty acids in food, namely palmitic acid, stearic acid, oleic acid, and linoleic acid, and taking into account the most recent formation factors of Horvatovich and others (2005) of 1.4 nmol for the saturated 2-ACBs and 0.9 nmol for the unsaturated 2-ACBs per mmol precursor fatty acid per kGy—as a first approximation the formation factor of the di-unsaturated 2-ACB from linoleic acid is set to be similar to that of the mono-unsaturated 2-ACB from oleic acid—the prediction leads to the following yields: for chicken meat containing about 12.5% edible fat with a composition of approx. 21% palmitic acid, 6% stearic acid, 32% oleic acid, and 25% linoleic acid, which has been irradiated at the maximum dose of 3 kGy, levels of 2ACBs amounts to about 11 μg 2-dDCB, 3 μg 2-tDCB, 10 μg 2-tDeCB, and 8 μg 2-tD2eCB per 100 g of fresh irradiated (3 kGy) chicken. For beef, for example, ground beef patties containing a maximum of 23% fat with a fatty acid composition of approx. 27% palmitic acid, 15% stearic acid, 43% oleic acid, and 3.8% linoleic acid, a similar calculation arrives at 36 μg 2-dDCB, 20 μg 2-tDCB, 37 μg 2-tDeCB, and 3 μg 2-tD2eCB per 100 g of fresh irradiated (maximum dose 4.5 kGy) beef. If a 20% loss in 2-ACBs after cooking (Crone and others 1992a) is anticipated and the actual mean intake of poultry (as given by Health Canada 2003) is about 62.1 g poultry per day, this intake would provide 0.08 μg 2-dDCB + 0.02 μg 2-tDCB + 0.08 μg 2-tDeCB + 0.06 μg 2-tD2eCB per kg body weight (kg bw) per day.This makes a total intake due to irradiated poultry of about 0.24 μg 2-ACBs / kg bw / day.

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Similar for beef with a daily intake of 23.2 g (Health Canada 2003), the consumption of irradiated beef would result in an intake of 0.10 μg 2dDCB + 0.06 μg 2-tDCB + 0.10 μg 2-tDeCB + 0.01 μg 2-tD2eCB per kg body weight per day. The total intake of 2-ACBs due to irradiated beef would thus amount to 0.27 μg 2-ACBs / kg bw / day. The daily intake by irradiated beef and poultry results in a value of 0.51 μg 2-ACBs / kg bw / day. Of course it should be taken into account that not all beef and poultry at present is being irradiated, and this can also not be expected in the near future. Only a very low percentage of beef and poultry is presently irradiated.The rough calculation shows a conservative value, which, however, could increase if higher radiation doses used for sterilization were to be applied and if other irradiated fatcontaining foodstuffs with considerable amounts of 2-ACBs would be consumed. This calculated daily intake of roughly 0.5 μg 2-ACBs / kg bw may be compared with the estimated uptake of acrylamide by, for example, fried food such as french-fried potatoes or potato crisps, the average value for the general population reported by the WHO (2002) being about ~ 0.3–0.8 μg acrylamide / kg bw / day. However, the toxicology database of acrylamide contains much information, whereas knowledge about the toxicological properties of 2-ACBs is still scarce.Already during the evaluation of the health aspects of certain compounds found in irradiated beef in the 1970s by FASEB, it was mentioned that metabolic and toxicological studies of the 2-ACBs presumably present in beef would be desirable (Chinn 1979b). At that time, 2-ACBs had not yet been identified in food, but only in triglycerides irradiated at high doses (60 kGy). The total daily intake of roughly 40 μg 2-ACBs per person per day surpasses the recently discussed threshold of toxicological concern (TTC) of 1.5 μg / person / day (Barlow and others 2001), which is used by the U.S. FDA for reviewing components of food contact materials with low exposures. So it may be prudent to collect more knowledge on the toxicological and metabolic properties of 2-ACBs in order to quantify a possible risk—albeit minimal. Knowledge about the metabolism of 2-ACBs is very restricted. Only one study about the fate of 2-ACBs in rats has been published (Horvatovich and others 2002b). Rats received a drinking fluid containing 0.005% 2-tDCB or 2-tDeCB daily for four months.The 2-ACBs could be identified in very low amounts in the adipose tissues of the rats (10-5 times the total quantity consumed). Less than 1% of the 2-ACBs ingested daily were excreted in the faeces. These results indicate that 2-ACBs are probably largely metabolized.Thus, further metabolic studies are desirable.

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Food Irradiation Research and Technology

Toxicological Safety of 2-ACBs Although the toxicological safety of irradiated meat and poultry has been studied extensively, far less data is available pertaining to the genotoxic potential of 2-ACBs, the chemicals that are formed by the radiolysis of triglycerides, phospholipids, and fatty acids. Controversy over the genotoxicity of the 2-ACBs started following the publication of preliminary data by Delincée and Pool-Zobel (1998) in which 2-dDCB at concentrations of 0.30–1.25 mg / ml in in vitro experiments induced DNA strand breakage in primary human and rodent colon cells using the Comet Assay.The authors’ study cautioned against interpretation of the results to infer that irradiated foods were carcinogenic and instead called for more study on the issue of 2-ACB genotoxicity (Delincée and Pool-Zobel 1998). The Comet Assay, although used extensively as a screening assay, has not been validated for the detection of weak genotoxins and can produce false-positive results due to the chromosome degradation that occurs as a result of non-genotoxic cell death (Health Canada 2003; Tice and others 2000). A retest of multiple 2-ACBs in the Comet Assay, in human HT-29 and HT-29 cl 19A cells at concentrations up to 400 μM, failed to detect significant levels of DNA strand breakage (Burnouf and others 2002). The genotoxicity of 2-ACBs was also studied in two human cell lines, HeLa and HT-29, using an alkaline unwinding procedure to quantify DNA strand breaks and Fpg-sensitive sites following the procedure proposed by Hartwig and others (1996). The frequencies of both DNA strand breaks and oxidative DNA modifications served as sensitive indicators of DNA damage.The results obtained thus far demonstrate that all of the test compounds that were investigated (2-tDCB, 2-tDeCB, 2-dDCB and 2-DCB) have cytotoxic effects in both cell lines at concentrations ⱖ100 μM.All of the 2-ACBs were also shown to induce oxidative DNA damage. In the case of 2-tDCB and 2-tDeCB, DNA damage occurred only at concentrations that were already highly cytotoxic, such that considerable fractions of the cells were no longer viable.The situation was different with 2-dDCB and 2-DCB, where oxidative DNA damage occurred at non-cytotoxic concentrations, making these results more relevant to the toxicological assessment (Burnouf and others 2002; Marchioni and others, 2004). Several 2-ACBs including 2-dDCB have also been tested in the Salmonella Mutagenicity Test (SMT), with no induction of mutations due to exposure to 2-ACBs using TA97, TA98, and TA100 tester strains being detected (Burnouf and others 2002). Other laboratories have focused their efforts on 2-dDCB, a prevalent 2-ACB in ground beef formed by the radiolysis of palmitic acid.Two studies investigated the ability of 2-dDCB to induce mutagenesis in the bacterial reverse mutation assays, with and

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without exogenous metabolic activation (Sommers 2003; Sommers and Schiestl 2004). No increase in the formation of mutants was observed in the SMT or the E.coli TRP Assay using tester strains WP2 [pKM101],WP2 uvrA [pKM101], TA98, TA100, TA1535, and 1537, which were in agreement with results published by Burnouf and others (2002). Gadgil and Smith (2004) also investigated the ability of 2-dDCB to induce mutations in the SMT using tester strains TA97,TA98,TA100,TA102, and TA1535, and failed to detect an increase in the formation of mutants as a result of 2dDCB exposures up to 1 mg / plate.Three laboratories have now failed to detect an increase in mutagenesis as a result of exposure to 2-dDCB, or multiple 2-ACBs, in the widely used and validated SMT and E. coli TRP Assays. In forward mutagenesis assays, an entire gene is a target for mutagenesis, as opposed to single nucleotide changes that are detected in the bacterial reversion tests. 5-Fluorouracil (5-FU)-resistant mutants in E. coli or Salmonella are formed when a null mutation is fixed within the DNA sequence of the 0.551 kb uracil-phosphoribosyltransferase gene, which would normally convert 5-FU to a toxic metabolite within the bacterium (Skopek and Thilly 1983). Sommers and Mackay (2005) failed to detect an increase in the formation of 5-FU mutants in E. coli following exposure to 1 mg / ml 5-FU, with or without exogenous metabolic activation. Gene expression profiling has also been used extensively for determination of genotoxic potential and is capable of identifying many genotoxins that are not detectable using bacterial reverse mutation assays. Transcription of RNA from the DNA damage-inducible UmuDC, RecA, DinD, and Nfo DNA genes of E. coli has been shown to increase following exposure to genotoxins (Orser and others 1995a, b). 2-dDCB was not able to induce gene expression from any of those gene promoters, as measured by increased ␤-galactosidase activity levels, at concentrations up to 1 mg / mL in E. coli SF1 containing each of the aforementioned promoter/␤-galactosidase reporter constructs, with or without exogenous metabolic activation (Sommers and Mackay 2005). This is in contrast to other carcinogens routinely present in foods including formaldehyde, dimethylnitrosamine, and aflatoxin B1 as shown by Orser and others (1995a, b). The Microtox™ system uses the bioluminescent marine microorganism Vibrio fisheri to measure the acute toxicity of chemicals or environmental samples, and has been commercially available since the 1980s as a primary toxicity screen. Gadgil and Smith (2004) examined the cytotoxicity of 2-dDCB in the Microtox Assay in order to make a comparative analysis between 2-dDCB and common GRAS food additives including the carbonyl compounds cyclohexanone and 2-nonenal. In the Gadgil

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Food Irradiation Research and Technology

and Smith (2004) study the EC50 values, the test compound concentrations that produced a 50% decrease in bioluminescence, were 21.7 ppm for 2-dDCB, 37.4 ppm for cyclohexanone, and 1.65 ppm for nonenal.The authors concluded that the acute toxicity of 2-dDCB was between that of carbonyl group containing GRAS food additives cyclohexanone and 2nonenal in the Microtox Assay.These results are conflicting with those of Burnouf and others (2002), who in growth inhibition studies with Salmonella typhimurium bacteria found clear cytotoxic effects for several 2-ACBs, particularly for 2-DCB. The toxic dose (37% survival) of 2dDCB was about 40 μM, but that of 2-DCB was only 4 μM (Marchioni and others 2004). In addition to tests in bacteria, 2-dDCB has also been tested for the ability to induce rearrangement of chromosomes in eukaryotic cells. The Yeast (Saccharomyces cerevisiae) DEL Assay measures a compound’s ability to cause genomic rearrangements, induced by DNA strand breakage, by restoration of a nonfunctional duplication of the his3 gene to functionality (HIS3+) by intrachromosomal (DEL) recombination (Sommers and Schiestl 2004).The assay does not produce false positives due to cell death because only recombination events in live cells are selected for. This is unlike the Comet Assay, which detects only the DNA strand break, not the actual genetic endpoint. Concentrations up to 5 mg / ml of 2-dDCB, which reduced cell viability to 28%, failed to induce genomic rearrangements in the Yeast DEL Assay (Sommers and Schiestl 2004). In contrast, carcinogens commonly present in food such as benzene and formaldehyde each induce increases in intrachromosomal recombination in the yeast-based test (Sommers and others, 1995).Very recent experiments using Comet Assay to measure DNA strand breaks and 24-color-Fluorescence-In-Situ-Hybridization to estimate chromosomal abnormalities indicated that 2-dDCB had a genotoxic potential and caused chromosomal aberrations in human colon cells (Knoll and others 2005).

2-ACBs and Tumor Promotion There have been very few studies on the ability of highly purified 2-ACBs to induce tumors in animals. Raul and others (2002) investigated the ability of 2-tDeCB and 2-tDCB to induce pre-neoplastic lesions (aberrant crypt foci) and tumors in the colons of Wistar rats. In that study, rats were fed 1% ethanol in water, or fed 1.6 mg/day 2-ACBs (about 6 mg / kg bw) dissolved in water that contained 1% ethanol as the 2-ACB solvent. The rats in each group were injected (intra-peritoneal) at weeks 2 and 3 with carcinogen azoxymethane (15 mg / kg bw), which induces pre-

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neoplastic lesions (ACFs) and tumors in the colons of rodents.The animals were sacrificed at 3 and 6 months and the colons examined for the total number of aberrant crypt foci, the number of crypts per foci, and actual tumor formation. Only a small number of rats, six per group, were used in the study. For each of the test groups, the number of ACF/cm in the distal colon were similar, with no difference in the total number of ACFs being evident. However, a statistically significant, but less than twofold, increase in the number of aberrant crypts per foci was observed in the 2-tDeCBtreated rats after six months, but not after three months.After six months, the total number of tumors in the colon was threefold higher in the 2-ACBtreated animals than in the AOM controls.The colons of four of six AOMcontrol rats exhibited only one small tumor (~6 mm3). Multiple tumors were observed in four and three of six animals treated with 2-tDCB or 2-tDeCB, respectively, whereas medium (6 < S < 25 mm3) and larger (>25 mm3) tumors were detected only in 2-ACB-treated animals. The possibility that one or more of the 2-ACBs at pharmacological doses could be tumor promoters prompted the authors to recommend further research into the tumor promotion phenomenon. Additional in vivo studies, using larger numbers of animals, with 2-ACBs incorporated into the feed of animals as opposed to drinking water, that use multiple 2-ACB concentrations are clearly warranted in order to more accurately assess the tumor-promoting potential of the 2-ACBs.

Diet and Tumor Promotion Although the tumor-promoting potential of the 2-ACBs has not been fully elucidated, the increases in the number of aberrant crypts and tumors in 2-ACB treated animals that received large doses of the carcinogen azoxymethane and the tumor promoter ethanol would not be totally unexpected. Raul and others (2002) speculated that the increase in the number of aberrant crypts observed in their study might be due to the interaction of the fatty acid derivatives with the epithelial cells of the colon.The impact of high levels of dietary fat and the risk of chronic disease, including colon cancer, have been well documented (Weisburger 1997). Udilova and others (2003) found that dietary oil components can induce oxidative stress, lipid peroxidation in membranes, cytotoxicity, and enhanced risk of colon cancer through regenerative cell proliferation. Oxidized beef fat has been shown to induce the formation of colon tumors in rodents (Yang and others 1998). Other colon tumor promoters found in meat and poultry products include oxidized heme, cholesterol, and cholic acid (Van der Meer-van Kraaij and others 2005; Yang and

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others 1998; Tseng 1996). Consumption of high concentrations of fat and fat derivatives causes formation of tumors in the colons of rodents. It is not surprising, therefore, that large doses of purified 2-ACBs might induce formation of tumors in the colons of rodents.

Conclusions Cancer in animals and humans has been associated with many factors including excessive consumption of fried, smoked, and barbecued meats and fish, pickled foods, and alcohol. Carcinogens such as formaldehyde, furan, acrylamide, nitrosamines, and benzene are naturally occurring in many foods, or formed as a result of thermal processing.Tumor promoters present (at milligram and gram quantities) in meat include lipids and oxidized lipids, hemes, and cholesterol. Because levels of 2-ACBs are present in sufficient (albeit μg) quantities to be considered an indirect food additive, assessment of their toxicological potential should be a priority in the science of food irradiation. It should also be recommended that any toxicological risk assessment pertaining to the 2-ACBs should be in the context of the total human diet and the potential benefit of food irradiation in reducing illnesses, hospitalizations, and deaths associated with foodborne illness. Paracelsus, the fifteenth-century philosopher and scientist, observed that all substances are poisons; it is only a matter of dose. Although it is almost impossible to prove the absolute safety of any food or food processing technology, it is difficult to conceive—considering the toxicological database—that radiation-pasteurized foods, including meat and poultry, pose a significant risk to human health when consumed as part of a healthful, well-balanced diet. This is true especially when compared to other, “more established” food processing and preservation methodologies that have been directly associated with the formation of cancers in animals and humans.

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Berglin EH, Carlsson J. 1986. Effect of hydrogen sulfide on the mutagenicity of hydrogen peroxide in Salmonella typhimurium TA102. Mutat Res 175:5–9. Barlow SM, Kozianowski G, Würtzen G, Schlatter J. 2001. Threshold of toxicological concern for chemical substances present in the diet. Food Chem Tox 39:893–905. Boyd DR, Crone AVJ, Hamilton JTG, Hand MV, Stevenson MH, Stevenson PJ. 1991. Synthesis, characterization, and potential use of 2-dodecylcyclobutanone as a marker for irradiated chicken. J Agric Food Chem 39:789–792. Burnouf D, Delincée H, Hartwig A, Marchioni E, Miesch M, Raul F,Werner D. 2002. Etude toxicologique transfrontalière destinée à évaluer le risque encouru lors de la consommation d’aliments gras ionisés. Toxikologische Untersuchung zur Risikobewertung beim Verzehr von bestrahlten fetthaltigen Lebensmitteln. Eine französisch-deutsche Studie im Grenzraum Oberrhein. Rapport final / Schlussbericht INTERREG II. Projet / Projekt No. 3.171. Marchioni E, Delincée H, Editors. Bundesforschungsanstalt für Ernährung, Karlsruhe, BFE-R—02-02.pp.1-198. Chinn HI. 1979a. Evaluation of the health aspects of certain compounds found in irradiated beef. I. Further toxicological considerations of volatile products. Federation of American Societies for Experimental Biology, Life Sciences Research Office, Bethesda, MD. Contract Rep. No. DAMD 17-76-C-6055, pp. 1–29. Chinn HI. 1979b. Evaluation of the health aspects of certain compounds found in irradiated beef. II. Possible radiolytic compounds. Federation of American Societies for Experimental Biology, Life Sciences Research Office, Bethesda, MD. Contract Rep. No. DAMD 17-76-C-6055, pp. 1–42. Crone AVJ, Hamilton JTG, Stevenson MH. 1992a. Effect of storage and cooking on the dose response of 2-dodecylcyclobutanone, a potential marker for irradiated chicken. J Sci Food Agric 58:249–252. Crone AVJ, Hamilton JTG, Stevenson MH. 1992b. Detection of 2-dodecylcyclobutanone in radiation-sterilized chicken meat stored for several years. Int J Food Sci Technol 27:691–696. Crone AVJ, Hand MV, Hamilton JTG, Sharma ND, Boyd DR, Stevenson MH. 1993. Synthesis, Characterisation and Use of 2-Tetradecylcyclobutanone Together with Other Cyclobutanones as Markers for Irradiated Liquid Whole Egg. J Sci Food Agric. 62:361–367. Dauphin J, Saint Lebe LR. 1977. Radiation chemistry of carbohydrates. Pp.131-195, In Radiation Chemistry of Major Food Components (PS Alias, AJ Cohen, Editors), Elsevier,Amsterdam. Delincée H, Pool-Zobel BL 1998. Genotoxic properties of 2-dodecylcyclobutanone, a compound formed on irradiation of food containing fat. Radiat Phys Chem 52:39–42. Delincée H, Pool-Zobel BL, Rechkemmer G 1999. Genotoxizität von 2-Dodecylcylobutanon. Pp. 262–269, In Lebensmittelbestrahlung (M Knörr, DAE Ehlermann, H Delincée, Editors), 5. Deutsche Tagung, Karlsruhe, Berichte der Bundesforschungsanstalt für Ernährung. 1112 Nov. 1998; BFE-R—99-01. EN 1785. 2003. Foodstuffs—detection of irradiated food containing fat—Gas chromatographic / mass spectrometric analysis of 2-alkylcyclobutanones, (revised version, supersedes EN 1785:1996). European Committee for Standardization, Brussels. Fan X,Thayer DW. 2002. Formation of malonaldehyde, formaldehyde, and acetaldehyde in apple juice induced by ionizing radiation. J Food Sci 67:2523–2528. Fan X. 2003. Ionizing radiation induces formation of malondialdehyde, formaldehyde, and acetaldehyde from carbohydrates and organic acid. J Agric Food Chem. 51(20): 5946–5949. Federal Register. 2005. Irradiation in the Production, Processing, and Handling of Food [Docket No. 1999F-4372] 21 CFR Part 199. Federal Register 70(175) 48057–49073.

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Fiddler W, Pensabene W, Gates RA, Jenkins RK,Wierbicki E. 1985. Observations on the use of gamma irradiation to control nitrosamine formation in bacon. Food Irradiation Processing: Proceedings International Symposium Food Irradiation Processing. Washington, D.C., 4–8 March, 1985, pp. 238–239. Friedman M. 2003. Chemistry, biochemistry, and safety of acrylamide.A review. J Agric Food Chem. 51(16):4504–4526. Gadgil P, Smith JS. 2004. Mutagenicity and acute toxicity evaluation of 2-dodecylcyclobutanone. J. Food Sci. 69:713–716. Gadgil P, Hachmeister KA, Smith JS, Kropf DH. 2002. 2-Alkylcyclobutanones as irradiation dose indicators in irradiated ground beef patties. J Agric Food Chem. 50:5746–5759. Handel AP, Nawar WW. 1981. Radiolytic Compounds from Mono-, Di- and Triacylglycerols. Radiat Res 86:428–436. Hartwig A, Dally H, Schlepegrell R. 1996. Sensitive analysis of oxidative DNA damage in mammalian cells: Use of the bacterial Fpg protein in combination with alkaline unwinding.Toxicol Lett. 88:85–90. Health Canada. 2002. Irradiation of ground beef: Summary of submission process. October, 29. Food Directorate, Food Products and Health Branch, Ottawa, www.hc-sc.gc.ca/foodaliment/fpi-ipa/e-gbeef_submission.pdf. Health Canada. 2003. Evaluation of the significance of 2-dodecylcyclobutanone and other alkylcyclobutanones. Pp. 1–7. http://www.hc-sc.gc.ca/food-aliment/fpi-ipa/e-cyclobutanone.html.Accessed September 2004. Horvatovich P, Miesch M, Hasselmann C, Marchioni E. 2002a. Supercritical fluid extraction for the detection of 2-dodecylcyclobutanone in low dose irradiated plant foods. J Chromatogr A 968:251–255. Horvatovich P, Raul F, Burnouf D, Delincée H, Hartwig A, Werner D, Marchioni E. 2002b. Detection of 2-alkylcyclobutanones, markers for irradiated foods, in adipose tissues of animals fed with these substances. J Food Protect 65:1610–1613. Horvatovich P, Miesch M, Hasselmann C, Delincée H, Marchioni E. 2005. Determination of mono-unsaturated alkyl side-chain 2-alkylcyclobutanones in irradiated foods. J Agric Food Chem, 53:5836-5841. Kim JH,Ahn HJ, Kim DH, JoC,Yook HS, Park HJ, Byun MW 2003. Irradiation effects on biogenic amines in Korean fermented soybean paste during fermentation. J Food Sci 68:80–84. Kim KS, Lee JM, Seo HY, Kim JH, Song HP, Byun MW, Kwon JH. 2004. Radiolytic products of irradiated authentic fatty acids and triacylglycerides. Radiat Phys Chem 71:45–49. Kim JK,Ahn HJ, Lee JW, Park JP, Ryu GH, Kang IJ, Byun MW. 2005. Effects of gamma irradiation on the biogenic amines in pepperoni with different packaging conditions. Food Chem 89:199–205. Knecht-van Eekelen A de, Mueller HC van den,Til HP, Groot AP de. 1971. Multi-generation study in rats with radiation-pasteurized chicken. Rept. R3622. Central Inst. For Nutrition and Food Research. Zeist,The Netherlands. Knecht-van Eekelen A de, Feron VJ,Til HP, Groot AP de. 1972. Chronic (two year) feeding study in rats with radiation-pasteurized chicken. Rept. R3773. Central Inst. For Nutrition and Food Research. Zeist,The Netherlands. Knekt P, Jarvinen R, Dich J, Hakulinen T. 1999. Risk of colorectal and other gastro-intestinal cancers after exposure to nitrate, nitrite and N-nitroso compounds: A follow-up study. Int. J Cancer. 80:852–856. Knoll N,Weise A, Glei M, Claussen U, Marian B, Pool-Zobel BL. 2005. 2-Dodecylcyclobutanone, a radiolytic product of palmitic acid, causes DNA strand breaks and chromosomal aber-

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rations in human colon adenoma cells. Naunyn-Schmiedeberg’s Arch Pharmacol. 371, Suppl. 1, R 131. Lee MS, Kim HL, Jeong, JB. 1973. Effects of ionizing radiation on development of wound periderm, solanine content, and the formation of carbonyl compounds in potato tubers. Korean J Food Sci Technol. 5:65–69. LeTellier PR, Nawar WW. 1972. 2-Alkylcyclobutanones from radiolysis of triglycerides. Lipids 1:75–76. Levin DE, Marnett L,Ames BN. 1984. Spontaneous and mutagen induced deletions: Mechanistic studies in Salmonella tester strain TA102. Proc Natl Acad Sci (U.S.A.) 81:4457–4461. Mufti SI. 1998.Alcohol-stimulated promotion of tumors in the gastrointestinal tract. Cancer Detect Prev. 22(3):195–203. Marchioni E, Raul F, Burnouf D, Miesch M, Delincée H, Hartwig A, Werner D. 2004. Toxicological study on 2-alkylcyclobutanones—results of a collaborative study. Radiat Phys Chem. 71:145–148. Matiella JE, Hsieh TCY. 1991.Volatile compounds in scrambled eggs. J Food Sci 56:387–390, 426. McNeal TP, Nyman PJ, Diachenko GW, Hollifield HC. 1993. Survey of benzene in foods by using headspace concentration techniques and capillary gas chromatography. J AOAC Int 76:1213–1219. Meier W,Artho A, Nägeli P. 1996. Detection of Irradiation of Fat-containing Foods by On-line LC-GC-MS of Alkylcyclobutanones. Mitt Geb Lebensm Hyg 87:118–122. Merritt Jr C,Angelini P, Graham R A. 1978. Effect of radiation parameters on the formation of radiolysis products in meat and meat substances. J Agric Food Chem 26:29–35. Nam KC, Min BR, Park KS, Lee SC,Ahn DU. 2003. Effects of ascorbic acid and antioxidants on the lipid oxidation and volatiles of irradiated ground beef. J Food Sci 68:1680–1685. Nawar WW. 1978. Reaction mechanisms in the radiolysis of fats: A review. J Agric Food Chem 26:21–25. Nawar WW. 1986.Volatiles from food irradiation. Food Reviews Intern 21:45–78. Ndiaye B. 1998. Les 2-Alkylcyclobutanones, molecules indicatrices d’un traitement ionisant des aliments. PhD Thesis, University Louis Pasteur Strasbourg. Ndiaye B, Jamet G, Miesch M, Hasselmann C, Marchioni E. 1999a. 2-Alkylcyclobutanones as markers for irradiated foodstuffs II.The CEN (European Committee for Standardization) method: Field of application and limit of utilization. Radiat Phys Chem 55:437–445. Ndiaye B, Horvatovich P, Miesch M, Hasselmann C, Marchioni E. 1999b. 2-Alkylcyclobutanones as markers for irradiated foodstuffs. III. Improvement of the field of application on the EN 1785 method by using silver ion chromatography. J Chromatogr A 858:109–115. Nishimura H, Philp RP, Calvin M. 1977. Lipids of Hevea brasiliensis and Euphorbia coerulescens. Phytochemistry 16:1048–1049. Orser CS, Foong FC, Capaldi SR, Nalezny J, Mackay W, Benjamin M, Farr SB. 1995a. Use of prokaryotic stress promoters as indicators of the mechanisms of toxicity. In Vitro Toxicol 8 (1):71–85. Orser CS, Capaldi S, Morse R, Schnieder BJ, Nalezny J, Farr SB 1995b. Utility of cell wall mutants in the Pro-Tox bacterial stress gene assay. Xenometrix, Inc. 2860 Wilderness Place, Boulder, CO, 80301, U.S.A. Park ER, Kim EA, Kim KS. 2001. Detection of radiation-induced hydrocarbons and 2alkylcyclobutanones from irradiated pork. Food Sci Biotechnol 10:84–89. Perez-Locas C,Yaylayan VA. 2004. Origin and mechanistic pathways of formation of the parent furan—a food toxicant. J Agric Food Chem. 52:6830–6836.

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Poling CE, Warner WD, Humburg FR, Reber EF, Urbain WM, Rice EE. 1955. Growth, reproduction, survival and histopathology of rats fed beef irradiated with electrons. Food Res 20:193–214. Raul F, Gossé F, Delincée H, Hartwig A, Marchioni E, Miesch M,Werner D, Burnouf D. 2002. Food-borne radiolytic compounds (2-Alkylcyclobutanones) may promote experimental colon carcinogenesis. Nutr Cancer 44:188–191. Reyns KM, Diels AM, Michiels CW. 2004. Generation of bactericidal and mutagenic components by pulsed electric field treatment. Int J Food Microbiol 93(2):165–173. Skopek TR, Thilly WG. 1983. Rate of induced forward mutation at 3 genetic loci in Salmonella typhimurium. Mutat Res 108:45–56. Smith CM, Koch WH, Franklin SB, Foster PL, Cebula TA, Eisenstadt E. 1990. Sequence analysis and mapping of the Salmonella typhimurium LT2 umuDC operon. J Bacteriol 172:4964–4978. Smith JS, and Pillai S. 2004. Irradiation and food safety. Food Technology 58 (11):48–55. Sommers CH, Mackay WJ, Nalezny J, Gee P, Benjamin M, Farr SB. 1995. Induction of DEL recombination in the yeast Saccharomyces cerevisiae using a microtiter plate format. In Vitro Toxicol 11:37–47. Sommers CH. 2003. 2-Dodecylcyclobutanone does not induce mutations in the Escherichia coli tryptophan reverse mutation assay. J Ag Food Chem 51:6367–6370. Sommers CH, Schiestl RH. 2004. 2-Dodecylcyclobutanone does not induce mutations in the Salmonella Mutagenicity Test or intrachromosomal recombination in Saccharomyces cerevisiae. J Food Prot 67:1293–1298. Sommers CH, Mackay WM. 2005. 2-Dodeclycyclobutanone does not induce formation of 5fluorouracil resistant mutants or increase expression of DNA damage inducible genes in Escherichia coli. J Food Sci 70:254–256. Stevenson MH, Crone AVJ, Hamilton JTG. 1990. Irradiation detection. Nature 344:202–203. Stevenson MH. 1992. Progress in the identification of irradiated foods. Trends Food Sci Technol 3:257–262. Stevenson MH. 1994. Identification of Irradiated Foods. Food Technol 48:141–144. Stevenson MH, Crone AVJ, Hamilton JTG, McMurray CH. 1993.The use of 2-dodecylcyclobutanone for the identification of irradiated chicken meat and eggs. Radiat Phys Chem 42:363–366. Stevenson MH. 1996.Validation of the Cyclobutanone Protocol for Detection of Irradiated Lipid Containing Foods by Interlaboratory Trial, McMurray CH, Stewart EM, Gray R, Pearce J (Eds.). In Detection Methods for Irradiated Foods–Current Status. Pp. 269–284. Royal Society of Chemistry, Cambridge, UK. Stewart EM. 2001. Food Irradiation Chemistry. Molins RA (Ed.). In Food Irradiation: Principles and Applications. Pp. 37–76. J.Wiley & Sons, New York. Stewart EM, McRoberts WC, Hamilton JTG, Graham WD. 2001. Isolation of lipid and 2alkylcyclobutanones from irradiated foods by supercritical fluid extraction. J AOAC Int 84:976–986. Stewart EM, Moore S, Graham WD, McRoberts WC, Hamilton JTG. 2000. 2-Alkylcyclobutanones as markers for the detection of irradiated mango, papaya, Camembert cheese and salmon meat. J Sci Food Agric 80:121–130. Swallow AJ. 1991. Wholesomeness and safety of irradiated foods. Friedman, M. Editor. In Nutritional and toxicological consequences of food processing. Pp. 11–31. Plenum Press, NY, NY, U.S.A. Tanabe H, Goto M, Miyahara M. 2001. Detection of irradiated chicken by 2-alkylcyclobutanone analysis. Food Irrad Japan 36:26–32.

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Thayer DW, Christopher JP, Campbell LA, Ronning DC, Dahlgren RR, Thompson GM, Wierbicki E. 1987. Toxicology studies of irradiation-sterilized chicken. J Food Prot 50:278–288. Tice RR, Agerell E, Anderson D, Burlison B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu JC, Sasaki YF. 2000. Single cell gel/comet assay; guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35(3):206–221. Tran TT, Medline A, Bruce WR. 1996. Insulin promotion of colon tumors in rats. Cancer Epidemiol Biomarkers Prevent 5:1013–1015. Tseng TH, Hsu JD, Chu CY,Wang CJ. 1996. Promotion of colon carcinogenesis through increasing lipid peroxidation induced in rats by a high cholesterol diet. Cancer Lttrs 100:81–87. Udilova N, Jurek D, Marian B, Gille L, Schulte-Hermann R, Nohl H. 2003. Induction of lipid peroxidation in biomembranes by dietary oil components. Food Chem. Toxicol. 41:1481–1489. U.S. Food and Drug Administration. 1997. Irradiation in the production, processing and handling of food. Final Rule. Federal Register 62 (232):64107–64121. Van der Meer-van Kraaij C, Kramer E, Jonker-Termont D, Katan MB, van der Meer R, Keijer J. 2005. Differential gene expression in rat colon by dietary heme and calcium. Carcinogenesis 26:73–79. Weisburger JH. 1997. Dietary fat and the risk of chronic disease: Mechanistic insights from experimental studies. J Amer Dietetic Assoc 97: 16–23. Weisburger JH, Jones RC. 1990. Prevention of formation of important mutagens/carcinogens in the human food chain. Basic Life Sci 52:105–118. World Health Organization. 1994. In Safety and nutritional adequacy of irradiated food. World Health Organization. Geneva, Switzerland, p. 81–107. World Health Organization. 2002. Health implications of acrylamide in foods. Report of a joint FAO/WHO consultation.World Health Organization. Geneva, Switzerland, Chapter 5, p.7-12. Yang CM, Kendall CWC, Stamp D, Medline AM,Archer MC, Bruce WR. 1998.Thermally oxidized dietary fat and colon carcinogenesis in rodents. Nutr Cancer 30:69–73.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 5 CONSUMER ACCEPTANCE AND MARKETING OF IRRADIATED FOODS Ronald F. Eustice and Christine M. Bruhn

Introduction Many innovations, even those with obvious advantages, require a lengthy period of time between when they become available and when they are widely accepted (Rogers 1983). Technologies such as pasteurization, immunization, and chlorination are now considered by health experts to be “pillars of public health,” yet each of these lifesaving innovations was met with suspicion and resistance when first introduced. Louis Pasteur discovered that bacteria could be eliminated by heating during the 1850s.This process became known as pasteurization and was highly controversial at that time. As late as the 1930s, many in the dairy industry resisted widespread use of pasteurization. One of multiple concerns expressed was that the promotion of pasteurized milk would cast a negative shadow over the nonpasteurized product and force milk handlers to install “expensive” equipment to pasteurize milk. During the 1920s, the U.S. dairy industry and insurance companies were promoting so-called certified raw milk as a more acceptable alternative to pasteurization (Metropolitan Life 1923). It was only through the insistence of medical and scientific groups that the dairy industry abandoned its “good milk” versus “bad milk” concerns and embraced pasteurization as a lifesaving technology that would help to make all milk safe. Pasteurization took nearly 70 years to be fully accepted in the United States, and the arguments against it were almost identical to those used today against food irradiation (Hall and Trout 1968).Among some 70 concerns raised by the critics of pasteurization were the following: 63

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• • • • •

“We must not meddle with nature.” “This process changes the properties of the food.” “Dangerous substances could be formed.” “This process could be carelessly done and accidents could happen.” “Pasteurization will increase the price of the product.We have a direct and prompt food distribution system.” • “It is not necessary.” None of these doomsday predictions turned out to be true; however, the campaign against pasteurization, including resistance from dairy producers and processors, significantly delayed its introduction, with the effect that thousands of people suffered chronic illness, developed longterm health consequences, or died. The question of legal responsibility for inflicting this suffering was never explored.

Resistance to “New” Technology Although food irradiation, sometimes called “cold pasteurization,” has been described as the “most extensively studied food processing technology in the history of humankind” and is endorsed or supported by virtually all medical and scientific organizations (see Table 5.1), the process is still considered a relatively “new” technology. It is human nature to resist change and to fear the “unknown.” Exploration of the “new world” was stifled by critics who believed the earth was flat. Arguments against constructive change take many forms. University of Houston economics professor and noted author Thomas R. DeGregori says,“One common argument against change is the search for a risk less alternative” (DeGreggori 2002). DeGregori says,“Every change has its risks; some real, others imagined.Whether a change is political, scientific, or technological, a simple assertion of risk should not in and of itself be an argument against that change.We must measure the benefits of change against the risks of not changing.” Christopher Columbus and other explorers faced a multitude of risks, but their ships did not drop off the edge of the earth. Impossible demands for a zero-risk society are often made by those who wish to maintain the status quo and convince others that the risks outweigh benefits.Those who choose to believe that the earth is flat despite overwhelming scientific evidence to the contrary have every right to do so. In a free society, proponents of the “Flat Earth Theory” have a right to their own set of opinions, but those opinions do not alter the fact that the earth is demonstrably and unequivocally spherical.

Table 5.1.

List of Organizations That Approve or Endorse Irradiation

American Council on Science and Health American Dietetic Association American Farm Bureau Federation American Feed Industry Association American Meat Institute American Medical Association American Veterinary Medical Association Animal Health Institute Apple Processors Association Centers for Disease Control & Prevention Chocolate Manufacturers Association Codex Alimentarius Council for Agricultural Science and Technology Florida Fruit and Vegetable Association Food and Drug Administration Food Distributors International Food and Agriculture Organization (FAO) Grocery Manufacturers of America Health Physics Society Institute of Food Science & Technology Institute of Food Technologists International Atomic Energy Agency International Food Information Council (IFIC) The Mayo Clinic Millers' National Federation National Confectioners' Association National Cattlemen's Beef Association National Food Processors Association National Fisheries Institute National Meat Association National Food Processors Association National Turkey Federation National Pork Producers Council Northwest Horticulture Association Produce Marketing Association Scientific Committee of the European Union United Egg Association United Fresh Fruit & Vegetable Association United Egg Producers United Kingdom Institute of Food Science & Technology United States Chamber of Commerce U.S. Department of Agriculture Western Growers Association World Health Organization (WHO)

65

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Risks versus Benefits DeGregori says,“If we examine the many changes over the past century— changes that have reduced infant and child mortality by more than 90%, have given Americans nearly 30 years of added life expectancy, have recently caused an even more rapid growth in disability-free years of life, and have allowed comparable or greater advances in other countries— we will find that all those changes carried risks.” Technologies such as chlorination of water, pasteurization of milk, synthetic fertilizers, chemical pesticides, modern medicine, genetically enhanced organisms, immunization, and irradiation, to name a few, all faced and continue to face various levels of opposition. Most cities use chlorine to purify their water, most parents want their children immunized against dreaded diseases, and very few people would consider drinking unpasteurized (raw) milk because of the known risks. Yet these lifesaving technologies all have their risks. Chlorine is toxic, and immunization can sometimes cause the disease it was intended to prevent. Pasteurized milk tastes different than milk straight from the cow, can be recontaminated, and will spoil if not refrigerated. By comparison, the risks of irradiation, if there are any, are “unknown” because after years of study, scientists haven’t found any (Wisconsin State Journal Editorial Board 2003). Weigh that against the known risks of contracting bacterial illnesses from the consumption of food that harbors unseen pathogens.

World’s Safest Food Supply, But Not Safe Enough The meat and poultry industry’s surveillance and intervention efforts have reduced, but not eliminated, microbial contamination of meat and poultry carcasses (CDC 2000; USDA FSIS 2003). Steve Kay, Editor and Publisher of Cattle Buyers Weekly, estimates that between 1993 and 2003, the 10 largest beef-processing companies spent more than $400 million on new equipment and added $250 million to their operating costs to fight E. coli O157:H7. Kay calculates that the overall cost of E. coli O157:H7 to the beef industry since 1993 is $2.8 billion and rising (Kay 2003). Despite these efforts, consumers continue to experience preventable illnesses and deaths caused by microbial contamination of foods. Traditional safety measures have the primary role in ensuring the safety of our meat supply, but they will not eliminate all contamination, particularly in a meat-processing environment. The U.S. Department of Agriculture’s (USDA) Food Safety and Inspection Service determined that

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the contamination level for E. coli O157:H7 in ground beef was 0.17% in 2004 compared to 0.30% in 2003, 0.78% in 2002, 0.84% in 2001, and 0.86% in 2000 (USDA 2005). Although this downward trend is very encouraging, it is imperative that the meat industry further enhance efforts to provide the public with the protection they expect and deserve against foodborne illness. Because the U.S. produces about 8 billion pounds of ground beef annually, even this exceedingly low percentage of contamination means production of an estimated 12 to 15 million pounds of E. coli O157:H7– contaminated ground beef each year (Roybal 2003). Based on these numbers, nearly two of every 1,000 hamburger patties produced in the U.S. contain bacterial pathogens when they leave the manufacturing plant. If that contaminated ground beef is not properly cooked to 160 degrees Fahrenheit (71 degrees Centigrade), it can cause serious injury or death. Furthermore, pathogens that may be on the meat could potentially contaminate other foods in the kitchen. If the product were irradiated, the pathogens would be destroyed before entering the home or foodservice kitchen. What would be the public response if a Detroit automaker sold a line of vehicles while fully aware that 0.17% of those vehicles had a production defect that each year could potentially lead to thousands of injuries and scores of deaths among its customers? The situation becomes more serious when we consider recent research by FDA/FSIS that shows that although some 60% of households have a meat thermometer, only 6% of consumers report using it often or always (Cates, 2002). Research at Utah State University further confirms this data (Anderson and others, 2004).The study, completed in 2003 and published in the Journal of the American Dietetic Association, showed that only five of 99 participants used a thermometer to determine doneness of meat, poultry, or seafood and only six of those who owned a thermometer reported using it often/always. Nearly half of study participants reported not knowing the recommended cooking temperature for chicken (43%) and ground beef (44%).

Irradiation: A Powerful and Effective Tool to Improve Food Safety Although irradiation cannot prevent primary contamination, it is the most effective tool available to significantly reduce or eliminate harmful bacteria in raw product and make sure that contaminated ground beef does not reach the marketplace.At doses that are commonly used to ir-

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radiate ground beef, we can expect the following levels of pathogen reduction: E. coli O157:H7 99.99% to 99.9999% Salmonella 99% to 99.9% Listeria 99.9% to 99.99% Food irradiation has the potential to dramatically decrease the incidence of foodborne disease and has earned virtually unanimous support or approval from international and national medical, scientific, and public health organizations, as well as food processors and related industry groups. Dr. Robert Tauxe of the U.S. Centers for Disease Control and Prevention estimates that if 50% of poultry, ground beef, pork, and processed meats in the United States was irradiated, the potential benefit of the irradiation would be a 25% reduction in the morbidity and mortality rate caused by these infections. This estimated net benefit is substantial; the measure could prevent nearly 900,000 cases of infection, 8,500 hospitalizations, more than 6,000 catastrophic illnesses, and 350 deaths each year (Tauxe 2001). Given the probable number of unreported and undetected foodborne illnesses, this reduction is likely to be even greater (Table 5.2). The globalization of trade in food and agricultural commodities and the increasing demand for food safety and security from “Farm to Fork” represent new challenges to the food industry (Satin 2003). Morton Satin, former Chief of Food and Agro-Industries, FAO, Rome, Italy, describes the dismantling of national barriers to trade as opportunities for greater efficiencies in economic growth, but says that as free trade increases, foodborne disease organisms cross international borders with relative impunity. Satin says,“Pathogens journey along with finished food products, raw agricultural commodities, handlers, travellers, and hidden insects. When one considers that these organisms travel with the tiniest particles of dust carried in the wind and are easily swept along international waterways, it is apparent that even the most rigorous quarantine procedures cannot prevent the movement of foodborne pathogens between countries. Routine use of irradiation of fruits, vegetables, and raw meat at border crossings should be seriously considered as an intervention strategy.”

Consumer Acceptance of Irradiated Foods So, if irradiation is such a great idea, where can we buy irradiated foods? Why aren’t supermarket shelves full of irradiated meat and produce? Why aren’t restaurants serving irradiated hamburgers and poultry as a routine

Consumer Acceptance and Marketing of Irradiated Foods Table 5.2. Pathogen

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Food Irradiation: Potential Annual Public Health Benefits by Specific

Pathogen

Prevented Cases

Prevented Hospitalizations

E. coli O157:H7 and other STEC 23,000 Campylobacter 500,000 Salmonella 330,000 Listeria 625 Toxoplasma 28,000

700 2,600 4,000 575 625

Total

8,500

881,625

Prevented Major Complications

Prevented Deaths

250 HUS cases 250 GBS cases 6,000 RA cases 60 miscarriages 100-1,000 cases Cong. toxo 6,660 major illnesses

20 25 140 125 94 404

R.Tauxe, CDC. 2001.

part of doing business? When will state health departments recommend that all ground beef and poultry served in hospitals, day care centers, and nursing homes be irradiated? When will school boards that would never consider serving raw milk in school cafeterias demand that all ground beef and poultry served to students be precooked or irradiated? Although irradiated fruits, vegetables, and poultry have been available commercially on a limited basis since the early 1990s, the introduction of irradiated ground beef in Minnesota during May 2000 significantly increased awareness and interest in the technology.According to Jim Jones, Food Tech Services, Mulberry, FL, approximately 18 to 20 million pounds of irradiated ground beef and poultry were marketed in the United States during 2004. Jones also estimates that some 2 million pounds of irradiated fruits and vegetables, mainly mango, papaya and guava, are sold annually by U.S. retailers. Spices have been commercially irradiated since 1986.Approximately one-third of the commercial spices consumed in the United States, some 175,000,000 lbs, are irradiated annually according to John Masefield, Executive Advisor of Steris IsoMedix Services, Mentor, OH. Yet, despite widespread media attention from food recalls, serious illness, and death, food irradiation technology remains underutilized and often misunderstood. Acceptance of irradiation has been slowed by several factors (Osterholm and Norgan 2004). First, the term “irradiation” is sometimes confusing or alarming to consumers because of its perceived association with radioactivity. Second, the causes, incidence, and prevention of foodborne disease are poorly understood by the general public.Third, health professionals and the media are largely unaware of the benefits of food irradia-

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tion. Finally, an anti-irradiation campaign has been conducted by certain activist groups because of their beliefs about food production issues, nuclear power, international trade, and industrialization, as well as the introduction of technologies.

Education: The Key to Consumer Acceptance What is preventing the technology from gaining widespread consumer acceptance? Numerous consumer studies clearly show that when given a choice and even a small amount of accurate information, consumers are not only willing to buy irradiated foods but also often prefer them over food treated by conventional means.A variety of market research studies conducted over the past two decades repeatedly demonstrate that 80–90% of consumers will choose irradiated products over nonirradiated after they hear the facts and understand the benefits. In a 1995-1996 University of California, Davis, study, interest in buying irradiated foods among California and Indiana consumers increased from 57% to 82% after seeing a 10-minute video describing irradiation. A 1995 study at Kansas State University showed that more than 80% of 229 respondents would purchase irradiated instead of nonirradiated poultry if both were offered at the same price.Thirty percent were prepared to pay a 10% premium for irradiated chicken, and 15% indicated a willingness to pay a 20% premium. A 2001 study funded by the Cattlemen’s Beef Board (CBB) (National Cattleman’s Beef Association 2002) showed that consumer acceptance of irradiated ground beef is growing.The study, which measured consumer perceptions about irradiated ground beef, revealed a sizeable potential market for the product. Researchers found that a person’s acceptance of irradiated beef was greatly influenced by initial perceptions. Four consumer segments were identified: strong buyers (27% of the test group), interested (34%), doubters (24%), and rejecters (15%). The first three were identified as potential markets for irradiated ground beef, and the study suggested that by implementing consumer education programs and continuing product quality research, the market for irradiated ground beef should continue to grow. Nearly all the “strong buyers” were ready to buy irradiated ground beef before the study, more likely to buy it after trying it, and willing to pay 10 cents a pound more for it.The “rejecter” segment snubbed placebo ground beef patties—nonirradiated burgers that were labeled as irradiated in the study—as often as the irradiated patties. The study said that no amount of information would convince this group, which generally rejects any new product.

Consumer Acceptance and Marketing of Irradiated Foods

Figure 5.1. 2003).

71

Consumer willingness to buy and pay for irradiated ground beef (Aiew

A spring 2002 study by Texas A & M University (TAMU) (Aiew and others 2003) investigated Texas consumers’ knowledge and acceptance of food irradiation and the effects of information about food irradiation on consumer acceptance and willingness to pay for irradiated ground beef (Figure 5.1). Before the presentation of any information in the TAMU study, about half of the respondents indicated a willingness to purchase irradiated ground beef.After receiving information about food irradiation, 88.5% of the respondents were willing purchasers. Even more (94.12%) indicated a willingness to buy irradiated ground beef after a second set of information on food irradiation was presented. The willingness-to-buy percentages in the Texas A & M study appear higher than estimates from the FoodNet Population Survey (1998-1999) conducted by the Centers for Disease Control and Prevention (CDC). The CDC also estimate that at least half of consumers will buy irradiated food, if given a choice between irradiated and nonirradiated; also, if consumers are first educated about irradiation, about 80% will buy irradiated products. Scientists at the University of Georgia conducted a survey to determine current consumer attitudes toward irradiation after consuming irradiated ready-to-eat poultry meat products and to evaluate differences in consumer acceptance, if any, over a 10-year period (1993 versus 2003) (Johnson and others 2004). Surveys were completed by 50 consumers in

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the metro-Atlanta area. More than twice as many consumers were willing to buy irradiated products in 2003 than in 1993 (69% and 29%, respectively).The majority (66%) of the respondents were aware of irradiation; among these, 71% indicated that they were either “somewhat informed” or “had heard about irradiation, but do not know much about it.” Consumers in both studies expressed more concern for pesticide and animal residues, growth hormones, food additives, bacteria, and naturally occurring toxins than irradiation. Consumers expressed slight concern regarding irradiation; however, this concern had decreased significantly over the past 10 years. Approximately 76% preferred to buy irradiated pork and 68% preferred to buy irradiated poultry to decrease the probability of illness from Trichinella and Salmonella, respectively. The University of Georgia study also found that a fourth (24–25%) of all consumers said they would buy more beef, poultry, and pork if these were irradiated and labeled.This figure reflects an 80–85% increase, over the 10-year period, in the number of consumers who would buy more poultry and beef, respectively. Many (41–45%) respondents said they would pay a 1–5% premium for irradiated products, with a few more going as high as 6–10%. A 2003 study by Jefferson Davis Associates (2003) showed that 68% of 396 respondents in six Midwestern states were aware of irradiation and 78% considered irradiated ground beef a “good thing.” The results of dozens of studies at leading universities consistently show that information about the nature and benefits of irradiation is a major factor affecting consumers’ perception of and attitudes toward irradiated foods.The findings reflect the importance of educating the public about the hazards of foodborne pathogens and the potential benefits of consuming irradiated foods. Studies consistently show that information plays an important role in consumer buying decisions, and consumers are generally receptive to irradiated foods when the benefits of irradiation are explained. Negative information about the process can reduce demand for irradiated foods, but that negative information can be honestly and effectively countered.

Effect of Unfavorable Information Fox and others (2001) describe how consumers respond to the presence of unfavorable information about food irradiation. In a choice experiment, 87 consumers were given a typical pork sandwich and asked to bid in a repeated auction for an upgrade to an irradiated pork sandwich. Participants were required to consume either the typical or the irradiated pork

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at the end of the experiment, and the auction was nonhypothetical—that is, the winner was required to pay for the upgrade to the irradiated pork. For the first five of a total of 10 rounds in the auction, participants were provided with a description of irradiation based on Food and Drug Administration information. Based on that description, approximately 60% of participants bid some amount to upgrade from a typical to an irradiated pork sandwich. The same participants were then provided with either a favorable or unfavorable description of irradiation, or both simultaneously.The favorable description (from the American Council on Science and Health) emphasized the benefits and safety of the process and its contribution to controlling foodborne illness.The unfavorable description (from Food & Water, Inc. a Vermont-based anti-irradiation advocacy group) noted that irradiation produced carcinogens called radiolytic products, that it caused vitamin losses, that it would eliminate warning signs of botulin toxin, and that the use of radioactive materials would put workers and nearby communities at risk. As expected, the favorable description alone resulted in more bids to upgrade to irradiated pork and the unfavorable description alone caused bids to decrease.When given only the favorable description, close to 90% of the participants bid for the upgrade to the irradiated product. Among those who were given only the unfavorable description, the proportion bidding for irradiated pork fell from 60% to 10–15%. But the disappointing result was that when subjects were provided with both sets of information, the effect of negative information dominated that of the positive and the proportion bidding for irradiated pork fell by approximately 20 percentage points. In fact, of 50 subjects who received both descriptions, only one subsequently submitted a higher bid to obtain an irradiated pork sandwich.

Can Unfavorable Information Be Counteracted? The results above demonstrate how negative information tends to dominate positive information and illustrates the need to honestly and aggressively counter false claims. Assuming that consumers will be exposed to unfavorable information about irradiation, this suggests that it is not sufficient for industry to promote food irradiation only on its own merits; it will also need to counter the claims made by opponents. The question then, is whether the anti-irradiation message can be effectively countered— that is, whether consumers, once exposed to anti-irradiation propaganda, can be reassured about the technology. To address that question, investigators conducted experiments in

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which consumers could purchase irradiated or nonirradiated chicken breasts. In the experiments (Shogren and others 1999; Fox 2002; Fox and others 2001), 96 consumers were provided with a U.S. Dept. of Agriculture brochure describing the food irradiation process and then asked to make a purchase choice between irradiated or nonirradiated (typical) chicken breasts. When all subjects had made their decision, they purchased and paid for the product they had chosen—and 79% purchased irradiated chicken. The participants were then provided with a copy of the unfavorable description of irradiation used in the earlier experiment and asked whether, if allowed, they would make a different purchase decision—and the proportion choosing irradiated chicken fell to 43%. Investigators were then interested to find out whether the negative claims could be countered and if confidence in the irradiated product could be restored.To counter the negative information, investigators used a televised report on food irradiation hosted by John Stossel of ABC News for the 20/20 news program.The report, entitled “The Power of Fear,”first broadcast on December 13, 1991, focused on protests at a food irradiation facility in Florida. Stossel interviewed the plant’s developer and representatives of Food & Water, Inc. who were leading the protest.The report concluded that food irradiation was a safe process, and Stossel indicated that, given the choice, he would actually prefer irradiated to nonirradiated meat. Furthermore, the report concluded that many of the claims made by Food & Water, Inc. were at best misleading or based on irrelevant science. Following the video segment, the investigators emphasized to the participants that (1) irradiated foods do not become radioactive; (2) radiolytic products, similar to those produced by irradiation, were also produced when foods were grilled or fried; (3) no studies had shown a connection between food irradiation and cancer or birth defects; (4) vitamin losses were insignificant and lower than those found in processes such as canning or freezing; (5) irradiation at approved doses did not sterilize food and spoilage warning signs were not lost; (6) there were no links between food irradiation and nuclear weapons or nuclear power; and (7) irradiation had been used to sterilize medical devices and consumer products for several decades with no problems related to the use or transportation of radioactive materials. Once again, investigators asked consumers to indicate what their purchase decision would be if they were allowed to repeat it—and 82% said they would choose irradiated chicken. These results illustrate that although the anti-irradiation message is powerful, it can be effectively counteracted and confidence in the safety of the irradiation process can be restored.

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Effects of Gender, Income, and Children Studies examining the effects of demographics on decisions to purchase irradiated food have found some consistent results. Typically, they find that females are more concerned about irradiation than males and, in most but not all cases, that individuals with more formal education are more accepting of the technology. Regarding the effects of age and income, results are mixed and generally not statistically significant (Lusk and others 1999). To determine the effect of gender, household income, and the presence of children, Fox and others examined results from two studies. First, the set of experiments referred to above in which consumers were exposed in sequence to positive, negative, and again positive information was examined, and the consumers were classified into different categories. Second, the results from a mail survey in which respondents made similar, albeit hypothetical, choices about purchasing irradiated chicken were examined. First, consistent with the results of other studies, males were more likely to be classified as proponents of irradiation. Second, the presence of children under 18 is associated with opposition to irradiation. Frenzen and others (2001) also reported a negative impact associated with the presence of children (under age 5), but their result was not statistically significant at the traditionally reported levels. Most studies find higher education associated with more favorable attitudes toward irradiation. It is worth noting that the effect of more education in the Kansas study showed more highly educated consumers more likely to be either “opponents” or “proponents” and less likely to be classified as “undecided.”This result is intuitively appealing because one does not generally associate opposition to technology with less education, and it may also explain why other studies do not always find a consistent linear impact for education. Finally, age of the respondent has no effect on classification, and, as expected, the higher the perceived risk from nonirradiated chicken, the more likely one is to be a proponent of irradiation.

Barriers to Acceptance The most significant obstacle to increased consumer acceptance of irradiated foods may well be the lack of availability in the marketplace.A survey of retail and foodservice beef purchasers was conducted in January and February 2004 by the National Cattlemen’s Beef Association to meas-

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ure awareness of, and attitudes toward, irradiation technology among foodservice and retail establishments that do and do not offer irradiated beef, measure the willingness to offer irradiated ground beef among those that do not offer it, identify barriers/issues to offering irradiated ground beef including researchable knowledge gaps, and both identify successful retailers and determine which practices help them sell this product (National Cattlemen’s Beef Association, 2004). The study showed that about four in 10 knowledgeable past users and nonusers of irradiated ground beef reported lack of availability as the main reason for not offering irradiated ground beef to their customers. This same study showed that respondents were relatively positive about purchasing irradiated ground beef. Almost half of past users were very (14%) or somewhat (33%) likely to purchase the product within the next year, and more than a fourth of the knowledgeable nonusers were very (4%) or somewhat (23%) likely to do so. In addition, a majority of the current purchasers (58%) indicated they would increase the amount of irradiated ground beef they would buy (versus 23% intending to decrease the amount).These data show a growing rather than a shrinking market.

The “Minnesota Model” of Consumer Acceptance Studies clearly show that an overwhelming majority of educated consumers will buy and in many cases prefer irradiated food products.These studies also point out a growing need to educate the public about the benefits of irradiation. The educational effort that began in Minnesota during the fall of 1997 has helped pave the way toward the successful introduction of irradiated ground beef and other foods not only in the United States but also a growing number of foreign countries. Following the largest recall of ground beef in history, Minnesota health experts, beef industry officials, and educators began to present consumers, opinion leaders, and others with facts and solid science about irradiation through a series of educational activities, product sampling demonstrations, information workshops, press releases, and media interviews. For example, in 1998, when John Glenn flew into outer space on Shuttle Discovery to help research how weightlessness affects the body of an older person, the Minnesota Beef Council sent out a press release calling attention to the fact that NASA has served irradiated foods in space since 1972. A team of experts from the Minnesota Department of Health, the University of Minnesota, and the food industry were quick to hold the critics accountable by challenging misinformation, half truths, and dis-

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torted information about irradiation through letters to the editor, opinion pieces, and media interviews. No opportunity was missed to serve samples of irradiated ground beef and inform the public about the benefits of food irradiation. More than 500,000 samples of irradiated ground beef have been served to consumers at various events in Minnesota and 30 other states since 1999.An Irradiated Ground Beef Education Initiative was conducted by the American National Cattlewomen during 2003 and 2004. The project involved product sampling and educational activities at women’s expos, food shows and other events to increase the knowledge of irradiated ground beef. More than 260,000 consumers/influencers were reached at 61 events in 20 states. Survey results were obtained from over 7,000 respondents and showed the following: • The majority of respondents (74% of 4,668) correctly said that irradiation does not eliminate the necessity for safe food handling practices. • The overwhelming majority (87% of 4,603) of respondents correctly stated that irradiation does not change the nutritional value of ground beef. • Ninety percent of 4,463 respondents correctly said that irradiation raises the food safety level of ground beef. • An unexpected finding was that almost half of respondents (46% of 4,728) did not know the proper cooking temperature for ground beef. • About 98 percent of respondents (3,286 out of a total of 3,347) at 25 events tabulated rated the taste of the irradiated ground beef samples with a positive score.The most frequent response was Good (1,382), followed by Great (335),Tasty/Very Good (186), and Excellent (168).A neutral score was given by 48 respondents (1.4%) with 22 respondents rating the product as Average. Negative evaluations were given by 25 individuals (0.7%).The average score was 8.2 on a 10-point scale. These informal taste tests combined with research at the University of Minnesota (Vickers and Wang 1999) have clearly demonstrated that irradiated ground beef is just as flavorful as typical, nonirradiated ground beef. A survey conducted at the 2001 Minnesota State Fair showed that only 39 percent of 201 participants would buy irradiated ground beef without sampling it first.After tasting the irradiated ground beef at the state fair, 89 percent said they would be willing to purchase irradiated ground beef.The importance of education, product sampling, and public/private partnerships is further confirmed by the previously mentioned Jefferson Davis Associates study (Shogren and others 1999) showing that 85% of

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Figure 5.2.

Food Irradiation Research and Technology

Overall appeal of irradiated beef concept (Jefferson Davis Associates, Inc.).

Minnesota respondents consider irradiated ground beef a “good thing,” compared to 78% overall (Figure 5.2). Irradiation education continues to be a major focus of a cooperative effort among the Minnesota Department of Health, the Minnesota Beef Research & Promotion Council, and ground beef manufacturers.Today, irradiated ground beef is readily available at most Minnesota supermarkets and many convenience stores, via home delivery and through mail order.

Marketing of Irradiated Ground Beef Louis Pasteur said,“To those who devote their lives to science, nothing can give more happiness than making discoveries, but their cups of joy are full only when the results of their studies find practical applications.” Pasteur did not live long enough to realize the magnitude of the impact resulting from his efforts. Neither did Marie Curie, whose landmark research on radiant energy and radiation earned her a Nobel Prize in 1904 and set the stage for the use of irradiation of food and medical products (Waltar 2004). In May 2000 Huisken Meats of Sauk Rapids, Minnesota, became the first ground beef processor in the nation to market irradiated ground beef when irradiated frozen ground beef patties were offered in 84 supermar-

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kets in the Twin Cities of Minneapolis/St. Paul, Minnesota. Schwan’s, Inc., a nation-wide foodservice provider through home delivery, quickly followed Huisken’s lead when it started marketing irradiated ground beef a few weeks later. Omaha Steaks of Nebraska has successfully marketed irradiated ground beef through mail order since 2000.Today, all noncooked ground beef offered by Schwan’s, Omaha Steaks, and several others is irradiated.Auburndale, Florida–based Colorado Boxed Beef offers frozen irradiated beef patties at about 1,000 supermarkets on the East Coast. In November 2004, a Cedar Rapids, Iowa–based company introduced irradiated fresh ground beef with extended shelf life at a number of convenience stores in Iowa and Illinois. In early 2005, it was estimated that irradiated ground beef (mostly frozen) was available in some 2,500 to 3,500 supermarkets and convenience stores. Rochester, New York–based Wegmans, with 68 supermarkets in New York, New Jersey, Pennsylvania, and Virginia, is a strong believer in the irradiation process and is one of the most visible marketers of irradiated ground beef.Although Wegmans takes every measure to ensure that all its ground beef products are safe, the retailer views irradiation as a value-adding process that offers the consumer an additional layer of food safety protection. Retailers throughout the United States have continued to show considerable interest in Wegmans’ successful marketing of irradiated ground beef.

A Defining Moment in Food Safety The successful commercial introduction of irradiated ground beef and poultry in supermarkets has gone largely unnoticed. According to food safety expert Morton Satin, when irradiated ground beef was introduced, consumers gained a reasonable expectation of buying products that offered much greater food safety and lower risk. As a consequence, untreated ground beef acquired the character legally defining a product having a built-in defect (Osterholm and Norgan 2004). Satin cites the American Legal Institute’s Third Restatement of the Law, Torts: Products Liability, adopted in 1998, which states in section 2, “Categories of Product Defect”: A product is defective when, at the time of sale or distribution, it contains a manufacturing defect . . . .A product: a) contains a manufacturing defect when the product departs from its intended design even though all possible care was exercised in the preparation and marketing of the product.

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Is it Farm to Fork, or Turf to Tort? Lawsuits and the threat of litigation as a result of recalls and sickness from E. coli 0157:H7, Salmonella, Listeria, and other pathogens will be a significant factor that will drive more retailers, restaurant chains, and manufacturers toward the use of irradiation (Eustice 2004).The financial liability for selling, using, lending, or simply having unsafe products on your premises rests with the business marketing the product.“If they sell it, they’re liable, period,” says Frances Zollers, a professor in the law and public policy department of the Whitman School of Management at Syracuse University in New York (Henricks 2005). For a victim, one case of foodborne illness is one too many. For a manufacturer, one recall is one too many. For a school district, one sick or dead child is a tragedy. For everyone but the attorneys prosecuting the case, one lawsuit is a nightmare! Faced with liability from selling contaminated products that can legally be defined as “defective,” the food industry will have to weigh the cost of using irradiation against the cost of product recalls, lawsuits, loss of brand equity, or even bankruptcy caused by such contaminated products (Satin 2003; Loaharanu 2003).

Conclusion No one single intervention can provide 100% assurance of the safety of a food product.That is why meat and poultry processing plants use a multiple barrier (hurdle) approach utilizing several types of interventions such as thermal processes combined with chemical and antimicrobial treatment to achieve pathogen reduction. These technologies have successfully reduced, but not eliminated, the amount of harmful bacteria in ground beef. Food irradiation does not eliminate the need for established, safe food-handling and cooking practices, but when used in combination with other technologies including an effective Hazard Analysis Critical Control Points (HACCP) program, irradiation becomes a highly effective

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and viable sanitary and phytosanitary treatment for food and agricultural products. Irradiation is one of the most effective interventions available because it significantly reduces the dangers of primary and crosscontamination without compromising nutritional or sensory attributes. The number of U.S. supermarkets that offer irradiated food at retail is significant and growing. Despite the progress made in the introduction of irradiated foods into the marketplace, many consumers and even highly placed policy-makers around the world are still unaware of the effectiveness, safety, and functional benefits that irradiation can bring to foods. Education and skilled marketing efforts are needed to remedy this lack of awareness. Morton Satin says, “Pathogens do not follow political imperatives or moral philosophies—they simply want to remain biologically active. Strategies to control them, which are based on political ideals or mythinformation, will not be effective. If we want to get rid of pathogens, we have to destroy them before they harm us. Food irradiation is one of the safest and most effective ways to do this.An international coordinated effort to develop effective knowledge transfer mechanisms to provide accurate information on food irradiation to policymakers, industry, consumers and trade groups is vital to meet today’s food safety needs” (Satin 2003). During the twentieth century, life expectancy in the United States increased from 47 to 77 years (CDC 2004). Many public health experts attribute this dramatic increase to the “pillars” of public health: pasteurization, immunization, and chlorination. Some of these same experts predict that food irradiation will become the fourth pillar of public health.Time will tell whether this prediction is correct.

References Aiew,W, Rudolfo, N, and Nichols, J. 2003.The Promise of Food Irradiation:Will Consumers Accept It? CHOICES. (Third Quarter 2003):31–34. Anderson, J, Schuster, T, Hansen, KE, Levy, AS, Volk, A. 2004. A Camera View of Consumer Food Handling Behaviors. Journal of American Dietetic Association: February 2004. Cates, S. 2002. Reported Safe Handling Practices: Cooking (FDA/FSIS Food Safety Survey2001). Changes in Consumer Knowledge, Behavior, and Confidence Since 1996 PR/HACCP Final Rule. Thinking Globally—Working Locally: A Conference on Food Safety Education, Orlando, FL, September 18, 2002. CDC. 2000. CDC Foodborne Outbreak Response and Surveillance Unit. Foodborne diseases outbreaks due to bacterial etiologies. (Accessed at: http://www.cdc.gov/foodborneoutbreaks/us_outb/fbo2000/bacterial00.htm.) CDC. 2004. National Center for Health Statistics, Centers for Disease Control and Prevention. Health: United States 2004 (Accessed on January 29, 2005 at: http://www.cdc. gov/nchs/data/hus/hus04trend.pdf#027)

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Consumer Reports. 2003. Of birds and bacteria. (Accessed on February 8, 2005 at: http://www.consumerreports.org/main/detailv2.jsp?CONTENT%3C%3Ecnt_id=29779 7&FOLDER%3C%3Efolder_id=162689) DeGregori, TR. 2002. Zero Risk Fiction. New York, NY: American Council on Science and Health. Eustice, RF. 2004.The Market for Irradiated Meat; Survey Reveals Lack of Knowledge: Meat & Seafood Merchandising. Lenexa, KS:Vance Publishing. p. 18–19. Fox, JA, Bruhn, CM, and Sapp, S. 2001. Consumer Acceptance of Irradiated Meats. In: Interdisciplinary Food Safety Research, Elsa Murano and Neil Hooker, eds. Boca Raton, FL: CRC Press. p. 139–158. Fox, JA. 2002. Influences on Purchases of Irradiated Foods. Food Technology 56 (11): 34–37. Hall, CW and Trout, GM. 1968. Objections to Pasteurization. In: Milk Pasteurization. Westport, Connecticut:The AVI Publishing Company. p. 5–8. Henricks, M. 2005. Risky Business; Before a Defective Product Becomes Your Downfall, Learn to Protect Yourself. In: Entrepeneur Magazine (March 2005) p. 32. Jefferson Davis Associates. 2003. Consumer Awareness of and Attitudes toward Irradiated Ground Beef. Presented to Mitec Advanced Technologies. Cedar Rapids, IA. 1–7. Johnson, A, Estes, RA, Jinru, C, and Resurreccion, AVA. 2004. Consumer Attitudes toward Irradiated Food: 2003 vs. 1993. Food Protection Trends 24(6): 408–418. Kay, S. 2003. Cattle Buyers Weekly. Meat & Poultry 49.2. Loaharanu, P. 2003. Irradiated Foods; Fifth Edition. American Council on Science and Health; New York. Lusk, JL, Fox, JA, McIlvain, CL. 1999. Consumer Acceptance of Irradiated Meat. Food Technology. 53(3):56–59. Metropolitan Life Insurance Company. 1923. All about Milk. New York: Metropolitan Life Insurance Company. p. 1–24. National Cattlemen’s Beef Association. 2002. Irradiation: Consumer Perceptions. On behalf of Cattlemen’s Beef Board, Centennial, Co. (Accessed on July 18, 2005 at: http://www. beefusa.org/uDocs/irradiation.pdf.) National Cattlemen’s Beef Association. 2004. Irradiation Beef Industry Study. National Cattlemen’s Beef Association on behalf of Cattlemen’s Beef Board, Centennial, Co. (Accessed July 18, 2005 at: http://www.beef.org/uDocs/Executive%20Summary %20Beef%20Industry%20Irradiation.pdf.) Osterholm, MT, Norgan, AP. 2004. The Role of Irradiation in Food Safety. New England Journal of Medicine, 2004 350(28):1898–1901 (Perspectives). Rogers, EM. 1983. Diffusion of Innovations, 3rd Edition. New York:The Free Press. Roybal, J. 2003. Beef industry logs successful week in E.coli O157:H7 battle. BEEF Magazine’s Cow-Calf Weekly. (Accessed September 30, 2003, at http://enews.primediabusiness.com/enews/beef/cowcalf_ weekly/current - a030926_4) Satin, M. 2003. Future Outlook: International Food Safety and the Role of Irradiation. International Meeting on Radiation Processing, Chicago, IL. Shogren, JF, Fox, JA, Hayes, DJ, and Roosen, J. 1999. Observed Choices for Food Safety in Retail, Survey and Auction Markets. American Journal of Agricultural Economics 81(5):1192–1199. Tauxe, RV. 2001. Food Safety and Irradiation: Protecting the Public from Foodborne Infections. Presentation from the 2000 Emerging Infectious Diseases Conference in Atlanta, Georgia. Emerging Infectious Disease 7(3): 516–521. Wisconsin State Journal Editorial Board. 2003. Let Irradiation Improve Safety Of School Food. Wisconsin State Journal, Madison. May 1, 2003.

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USDA FSIS. 2003. Food Safety and Inspection Service. 2003 recall cases. (Accessed at: http://www.fsis.usda.gov/OA/recalls/rec_actv.htm#2003) USDA FSIS. 2005. Press Release: FSIS Ground Beef Sampling Shows Substantial E. coli O157:H7 Decline In 2004. (Accessed at: http://www.fsis.usda.gov/News_&_Events/ NR_022805_01/index.asp on February 28, 2005) Vickers, Z, and Wang, J. 1999. Acceptability of Irradiated Fresh Ground Beef Patties; Influence of Information and Product Identification. University of Minnesota. Waltar, AE. 2004. Radiation and Modern Life, Fulfilling Marie Curie’s Dream. Amherst, NY: Prometheus Books.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 6 DETECTION OF IRRADIATED FOODS Eric Marchioni, Ph.D.

Introduction The action of ionizing radiation on food results in the formation of free radicals and radiolytic products that are predominantly not radiation specific. It was thus not astonishing that after many years of research before the nineties, it was still not possible to identify any specific radiolytic product that could be used to establish a universal analytical method for the detection of irradiated food. Moreover, the radiation process, when performed at usual absorbed doses (less than 10 kGy), involves many fewer chemical modifications than other treatments such as heating or storage. Indeed, the absorption of the maximal allowed dose for food irradiation (10 kGy) leads only to a temperature rise limited to 2.4° C.This observation pleads certainly in favor of the safety of radiation processing, but represents a major disadvantage when one seeks to identify such a process while studying physical or chemical modifications in the foodstuff itself. As a result of two concerted actions conducted and funded by the Community Bureau of Reference (Raffi and others 1993) and by the International Atomic Energy Agency (McMurray and others 1996) at the beginning of the nineties, no fewer than fifteen analytical methods for the detection of irradiated food were developed, of which ten were standardized by the European Committee for Standardization (CEN). Six of them are reference methods and are based on the analysis of primary radiolytic products, by electron spin resonance spectroscopy (ESR) (Anonymous 1996c, d; 2000a), and by thermoluminescence (Anonymous 1996e), or on the analysis of secondary radiolytic products from fatty acids, namely volatile hydrocarbons (Anonymous 1996a) and 2-alkylcyclobutanones (Anonymous 1996b). The four other methods resulting from these concerted efforts are less specific than the reference methods but are never85

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theless of interest because they are easier to carry out, less expensive, and less time-consuming than the reference ones and could thus be used as screening methods to establish a suspicion of irradiation treatment. It is recommended that any positive result obtained by such screening methods be confirmed using a standardized reference method. These screening methods consist in photo-stimulated luminescence (P.S.L.) (Anonymous 2000b), single gel micro-electrophoresis (Anonymous 2000c), bacteriological methods D.E.F.T./A.P.C. (Direct Epifluorescence Filter Technique/Aerobic Plate Count) (Anonymous 2000d) and L.A.L./ G.N.B. (Limulus Amoebocyte Lysate/Gram Negative Bacteria) (Anonymous 2004).The scope of all these methods is indicated in Table 6.1. Several bibliographical studies concerning the detection of irradiated food were already published (Hasselmann and Marchioni 1991; Delincée 1991; Raffi and others 1993; McMurray and others 1996).This chapter is a résumé of these various studies while insisting particularly on the methods selected and standardized by CEN, which have now been adopted by the Codex Alimentarius as General Codex Methods and which can be regarded today as being foolproof and effective. According to the chronological appearance of radiolytic products or changes observed in the food matrix, the methods for food irradiation detection can be classified according to the following two categories.

Free Radicals and Electronic Excited States ESR Spectroscopy Food having a dry or rigid matrix, or presenting certain dry or rigid parts, is able to trap free radicals or excited states of electrons for a period of time that can be much longer than the lifetime of the food itself.Thus, irradiated meat with bones (poultry, beef, pork, and so on), fish with bones, scales, or teeth, eggs with shells, shellfish, fruits with achenes, nuts with shells, dry fruits containing crystalline sugars, and some seeds and spices can be analyzed by electron spin resonance spectroscopy. It is a nondestructive analytical method that allows the detection of free radicals in matter. It consists in subjecting a test sample to the simultaneous action of a magnetic field (intended to direct the magnetic moments—spins— of the matter, and thus those of the free radicals) and of an electromagnetic microwave of very high frequency (approx. 9 GHz).When the value of the imposed magnetic field allows the spins of the radicals to be directed so that their transition energy becomes identical to that of the incident electromagnetic microwave, the energy of the latter is absorbed.

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Chemical methods

NF EN 13 783 D.E.F.T.-A.P.C.

Microorganism

Herbs and spices

(d)

(e)

Gram Negative Bacterium Fresh or frozen poultry meat

NF EN 14 569 L.A.L.-G.N.B.

Microbiological methods

(b) (c)

(a)

Screening Methods

(b) NF EN 1 784 NF EN 1 785 (c) Gas chromatography (d) Volatile hydrocarbon 2-Alkylcyclobutanone (e) Food containing fat

(a)

Reference Methods

Silicate and other mineral Food containing mineral debris, e.g. silicates

NF EN 13 751 P.S.L.

Food containing DNA

NF EN 13 784 Single gel microelectrophoresis DNA

Physical method Biochemical method

NF EN 1 788 NF EN 1 787 NF EN 1 786 NF EN 13 708 Thermoluminescence Electron spin resonance spectroscopy Silicate mineral Crystalline cellulose Bone, tooth, scale Crystalline sugar Food containing Food containing Food containing Food containing silicate minerals cellulose bones sugars

Physical methods

Table 6.1. Selected C.E.N. Methods for the Detection of Irradiated Food: (a) Type of Methods; (b) C.E.N. Classification; (c) Analytical Methods; (d) Compound to Be Analyzed; and (e) Application Field of the Method.

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Figure 6.1. ESR spectra 1) nonirradiated; 2) irradiated from samples of (a) 5 kGy irradiated poultry bones, (b) achenes extracted from 3 kGy irradiated strawberries, and (c) 5 kGy irradiated figs.

The derivative representation of this absorption, according to the value of the magnetic field, gives the ESR spectrum (Fig. 6.1). The application of this analytical method is simple, consisting of drying a food sample (water prevents the ESR analysis because of the O-H dipole, which absorbs the microwave energy) under reduced pressure at 50°C max in order to avoid modifying the food composition (sugars) and the recombination of the radicals, and to record the ESR absorption spectrum. Of course, the presence of radicals in food is not radiation specific (radicals are also produced by heating or crushing, and a low amplitude symmetric ESR absorption signal is also present in nonirradiated bone samples). Nevertheless, observing the shapes of the spectra recorded in case of irradiated samples, as well as their gyromagnetic factors, causes analysts to consider some ESR signals to be radiation specific. It is now widely recognized that the presence of ESR signals (as described below) is radiation specific, but the absence of such ESR signals (except in case of mammal bones) never constitutes proof that the food has not been irradiated. The spectrum presented in Figure 6.1a can be observed in irradiated food containing bones, fishbones, cuticles, teeth, or egg shells. It consists of an intense radiation-specific asymmetrical signal (A and B, g=2.002 g=1.998) superimposed upon a symmetrical endogenous signal (C, g=2.005) of much lower amplitude also present in nonirradiated bone samples (the beginning of this signal is presented in Figure 6.1a by the arrow S). It corresponds (Bacquet and others 1981) to an extremely stable

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CO2⭈– radical trapped in the lattices of hydroxyapatite [Ca10(PO4)6(OH)2] which constitutes approximately 60% of the bone composition. Measuring the ESR signals induced in animal bones is not really new. It has already been used for accidental post-irradiation dosimetry (Rossi and others 2000) and for dating bones and shells (Takano and Fukao 1994). Detection of irradiated fish and meat samples is generally possible above a minimal detectable dose of 0.5 kGy, lower than those used for commercial applications for this kind of food product. Identification remains possible up to 12 months after irradiation (Anonymous 1996c). The ESR signal represented in Figure 6.1b is obtained with irradiated food containing crystalline cellulose. It is a hyperfine triplet centered at g=2.004 and superimposed on an intense central nonradiation-specific singlet C belonging to lignin (Deighton and others 1993).This singlet has a similar g factor and is sensitive to radiation but also to drying processes (deJesus and others 1996). From the triplet ESR lines that are induced by irradiation, only the two outermost peaks A and B (g=2.020 and g=1.985, ⌬H~6mT) can be used in the case of very dry plant products such as paprika powder or dry fruit components (achenes, pips, shells, stalks, or stones) (Raffi and Agnel 1989) but also in citrus fruit skins, skin components and stalks (Tabner and Tabner 1994) and fruit cell walls (deJesus and others 1999; Delincée and Soika 2002). The multicomponent ESR signal in Figure 6.1c may be observed in some dry fruits containing crystalline sugars (raisins, mangoes, papayas) (Raffi and others 1992). As various mono- and disaccharides may widely be dominant in fruit samples, different ESR spectra, centered at g=2.003, could be produced after irradiation (Anonymous 2000a).They consist in intense and easily detectable multiplets that can be identified provided that the moisture has been correctly eliminated during sample preparation. Such nonirradiated foods containing crystalline sugars do not give out any ESR signal. Today, these three analytical ESR methods are CEN and Codex standards used by various EU Member States and also other countries all over the world to exercise control over the international trade of irradiated foods. Luminescence The absorption of ionizing radiation by matter induces the formation of electronic excited states. If the matter has a crystalline structure, the excited charge carriers can remain trapped in the crystalline lattice defects for several years. Heat stimulation (50°C to 500°C depending to the depth of the trap) releases a part of this stored energy in the form of detectable light. A thermoluminescence reader measures the amount of

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light that is emitted during controlled heating.This observation is already in use for radiation dosimetry including clinical applications, archaeological and geological age determination, mineral prospecting of uranium sources, study of meteorites and lunar material, or solid-state defect structure analysis.The use of thermoluminescence as a detection method for irradiated food first consisted in analyzing directly a few mg of the whole food sample (spices) with a commercial TL reader. In 1989 Sanderson reported that the origin of luminescence of spices is due to “extraneous inorganic matter.”The food is indeed almost always contaminated by very small quantities of silicate minerals, mainly quartz and feldspar (Soika 2000), which come either from the action of the wind (fruits with dust) or from the contact with soil (plants and spices with sand) or with the seabed (shells and shellfish with sand). The standardized CEN method (Anonymous 1996e) for the detection by thermoluminescence of food containing silicate minerals consists of water ultrasound-assisted extraction of the mineral impurities, separation of the silicate minerals from the organic fraction, and an analysis of the purified minerals by thermoluminescence. An irradiated foodstuff (Fig. 6.2) results in a sharp peak, approximately at 220°C, whereas nonirradiated food does not give out any TL signal at this temperature. Only some low signals caused by natural radioactivity appear beyond 350°C. Because mineral impurities are common to many food products, this method of analysis has wide applications.That is why this technique of detection is largely used in food control laboratories. Unfortunately, the equipment has no other application in an analytical food laboratory. A novel approach to this method was suggested by Sanderson and others (1996). These authors proposed to release the trapped charge carriers from their excited energy level using infrared pulsed laser beam excitation, which allows an examination of inorganic systems in the presence of organic matter. This technique is original because the energy carried by the emitted luminescence photon is higher than that of the laser excitation.This rare anti-Stokes property is highly radiation specific because the energy conservation principle lays down that the quantum energy differences between stimulation and luminescence are balanced by the energy stored in the form of trapped charge carriers.Therefore, nonirradiated samples are unable to participate in these transitions.The synchronous detection of the luminescence with the pulsation of the excitation laser light enhances the signal-to-background ratios, thus increasing detection sensitivity. Moreover, no preparation of the sample is necessary and the equipment appears as a simple box fitted with a drawer in which the food to analyze is introduced in a disposable petri dish.This fast and simple method was standardized by CEN (Anonymous 2000b). It is al-

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Figure 6.2. Thermoluminescence glow curves of silicate minerals extracted from a sample of dehydrated asparagus powder; (a) 8 kGy irradiated sample and (b) nonirradiated sample.

ready screening method is used in official national food control laboratories but also in several food industries and central buying offices. The radicals induced in foods by radiation processing can also be detected by indirect methods such as luminescence. The chemiluminescence consists of an emission of light consecutive to a chemical reaction. During rehydration of some irradiated dry foods, the radical recombination allows such light emission. This luminescence can be amplified by the use of additives such as Luminol or Lucigenine.This method was extensively studied by German authors (Bögl and Heide 1985) and was submitted for interlaboratory tests. However, it has a very poor reproducibility (Delincée 1987) and was not standardized by CEN.

Analysis of Stable Radiolytic Products After being induced in the food matrix, free radicals and excited states of the matter (extremely reactive chemical species of very short lifetime, ex-

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cept in the case of dry or/and rigid food) react with the food components, giving rise to a great number of chemical reactions and resulting in radiolytic products. In order to be detected in a foodstuff, the stability of these compounds must be comparable to the shelf-life of the food. Radiolytic Products from Proteins Detection of o-, m- and p-tyrosines, produced during radiolysis of food containing phenylalanine, was proposed by Simic and others (1983) who thought that o-tyrosine was a unique radiolytic product (U.R.P.). However, it was later shown by other authors (Hasselmann and Laustriat 1973; Hart and others 1988) that this molecule was also present in nonirradiated food and could also be formed by photolysis. Hein and others (1999) showed that o-tyrosine was indeed a natural product and thus could not be used as a food irradiation detection test except, of course, if a maximal threshold of o-tyrosine present in the food could be defined, a threshold above which the food is regarded as having been irradiated. In any case this method was never validated by blind tests or by interlaboratory analyses. Volatile Compounds The chromatograms of volatile food extracts (spices) present numerous peaks.The comparison (Hasselmann and others 1986; Swallow 1988) of such chromatograms from irradiated and nonirradiated food extracts highlights the presence or absence of peaks or the variation of some peak intensities. However, it was established that the profiling of these chromatograms depends also upon the origin of the analyzed spice and upon its treatments. Therefore a discrepancy between two chromatograms cannot be attributed to radiation treatment. Radiolytic Products from Carbohydrates The radiolysis of pure aqueous carbohydrate solutions is well described in the relevant literature (VonSonntag 1987). But the radiolysis of carbohydrates in food is much more complex.The process results in acids and carbonyl groups. Molecular weight or methylation degree changes leading to modifications of the viscosity of food extracts were also reported (Farkas and others 1990). But almost all the methods of detection based on the study of the carbohydrates radiolytic breakdown products were disappointing (Delincée and Ehlermann 1989), because the products observed were not radiation specific. Moreover, the variability of the radi-

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olytic product concentrations or of the food viscosity, depending on the food itself (origin, state of ripening, and conditions of culture and storage), was much higher than the variability that could be caused by the radiation process alone. Only the ESR analysis (Anonymous 2000a) as described at the beginning of this chapter allows an unambiguous detection of irradiated food containing crystalline sugars (dry fruits). Radiolytic Products from Nucleic Acids The presence of DNA in almost all food could be the basis of a universal method of detection of irradiated food. But the food DNA analysis is complex due to the low concentration of these fragile macromolecules.They quickly degrade when stored at temperatures above 0° C because of the nucleases present in the cells.This reduces the application field of this investigation to fresh or frozen food. Detection of chemical modifications of the bases was proposed by Pfeilsticker and Lucas (1987). These authors proposed a detection test based on the fluorescence analysis of thymine glycol, a thymine radioderivative.This work never could be confirmed by other laboratories because the production of this molecule is very dependent on the matrix of the studied food. Another very interesting study consists in an immunological detection of dihydrothymidine produced in absence of oxygen (radiation processing consumes oxygen dissolved in the cell) from thymidine (Williams and others 1994; Tyreman and others 2004). The fast and elegant method suggested by these authors was, however, not confirmed by other laboratories and no blind test was carried out to validate it. An original approach was proposed by Marchioni and others (1992). The suggested protocol is based on the morphological modifications of the mitochondrial DNA (mtDNA), which is protected against autolysis by the mitochondrial wall.The test thus remains applicable throughout the shelf life of food (in the fresh or frozen state). A low dose of irradiation (< 100 Gy) causes single strand breaks, which in turn transforms the native supercoiled mtDNA into an open circular mtDNA.An increase in the absorbed dose leads to the disappearance of the supercoiled shape, the multiplication of open circular mtDNA, and the appearance of linear shaped mtDNA. These three shapes may easily be separated by using agarose gel electrophoresis. Unfortunately, no other laboratory continued these studies, and the protocol suggested (quite long and complex) is not yet in use for the detection of irradiated food. The most successful approach was proposed by Östling (1988). This author proposed an extraction of the cells by a simple shaking in a buffer

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Figure 6.3. Electrophoretic pattern of single cells extracted from (a) nonirradiated and (b) 1.5 kGy irradiated poultry meat (H. Delincée).

solution.The cellular suspension, mixed with low-melt agarose, is coated on a microscope slide and subjected to short (2 min) electrophoresis.The cells whose DNA have a high molecular weight (unaltered DNA) will just migrate a little bit into the gel (Fig. 6.3a).The cells extracted from irradiated food have short DNA (because of strand breaks) and will migrate over longer distances (Fig. 6.3b). Electrophoretic pattern of such cells appears as comets whose heads are represented by the cell and the tails consist of the low molecular-weight DNA.The higher the absorbed dose, the longer the tail of the comet. This simple and fast method does not require any expensive equipment and can be used to analyze fresh or frozen foods. It is now a CEN standard (Anonymous 2000c), already used by several food control laboratories as a detection method of irradiated food. Radiolytic Products from Lipids Lipid radiolysis has been extensively studied (Nawar 1986, 1994) because the radiolytic breakdown products of edible fats (hydrocarbons, aldehydes, ketones, esters, peroxides, oxisterols, and so on) were suspected to degrade the flavor of irradiated food.As of now, only two analytical methods on lipids appear to be really interesting for the detection of irradiated food. The radiolysis of a fatty acid Cn:m (n = carbon atoms, m = double bounds) leads mainly, due to side chain breakage (␣ and ß position of the carbonyl group), to the formation of volatile hydrocarbons of formulas Cn-1:m and Cn-2:m+1, and of 2-alkylcyclobutanones, with a Cn-4 alkyl chain in position 2 of the four-carbon ring (Fig. 6.4 and Table 6.2). The presence of volatile hydrocarbons in a food, easily identified by gas chromatography with flame ionization detection, is not radiation spe-

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Figure 6.4. Radiation-specific breakages on the triglyceride molecule. (a) Cn-1:m hydrocarbon, (b) Cn-2:m+1, 1-unsaturated hydrocarbon, (c) 2-alkylcyclobutanone.

Table 6.2. fatty acids.

Radiolytic hydrocarbons and 2-alkylcyclobutanones from major food

Precursor fatty acid Palmitic (C16:0)

Stearic (C18:0)

Oleic (C18:1)

Hydrocarbon Pentadecane (C15:0) 1-Tetradecene (C14:1) Heptadecane (C17:0) 1-Hexadecene (C16:1) 8-Heptadecene (C17:1) 1,7-Hexadecadiene (C16:2)

2-Alkylcyclobutanone 2-Dodecylcyclobutanone (2-dDCB) 2-Tetradecylcyclobutanone (2-tDCB) 2-(Tetradec-5⬘-enyl)cyclobutanone (2-tDeCB)

cific, but the appearance in the chromatogram of a hydrocarbon couple Cn-1:m/Cn-2:m+1 for each corresponding fatty acid Cn:m establishes beyond doubt that the food analyzed has been irradiated (Fig. 6.5). The 2-alkylcyclobutanones are, until proof for the contrary is available, the first chemical compounds specifically formed by irradiation (Ndiaye 1999a).Their presence, corresponding to specific fatty acids (the 2-dodecylcyclobutanone, 2-tetradecylcyclobutanone, and cis 2-tetradec5’-enyl-cyclobutanone radio induced respectively from palmitic, stearic, and oleic acid) characterized by mass spectrometry after separation by gas chromatography (Fig. 6.6), thus is an unquestionable proof of a radiation process on the food analyzed (Stevenson 1990). The protocols proposed for the detection of hydrocarbons and 2-

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Figure 6.5. Chromatogram of volatile hydrocarbons extracted from 5 kGy irradiated milk powder (C14:1 and C15:0 induced from C16:0 palmitic acid, C16:1 and C17:0 induced from C18:0 stearic acid and C16:2, and C17:1 induced from C18:1 oleic acid).

alkylcyclobutanones are, in fact, very similar (Soxhlet extraction, SPE purification of the extracts on a Florisil column and separation by gas chromatography, with mass-selective detection in the case of the analysis of the 2-alkylcyclobutanones). The two standard protocols are applicable to food whose triglyceride content is not negligible (> 1g%), provided that the absorbed dose of radiation is not too weak (> 0.5 kGy) (Ndiaye 1999a). The chemical stability of volatile hydrocarbons and of 2-alkylcyclobutanones in food is quite good, and the moderate losses observed during storage do not reduce the validity of the two methods, which are now CEN standards (Anonymous 1996a,b).The application field of these methods is thus potentially very large. These standards have nevertheless the twofold disadvantage of being time consuming (1.5 to 2 days), partly owing to the use of a 6 h Soxhlet extraction, and quite expensive on account of the need for a large quantity of Florisil in the solid phase extraction needed to purify the extracts obtained (retention of the lipids). Horvatovich and others (2000) proposed the use of selective supercritical carbon dioxide extraction to reduce the duration of analysis (down to 3 hours) and to avoid the costly Florisil clean-up step. These authors succeeded in detecting and quantifying the two radiation-sensitive markers (hydrocarbons and 2-alkylcyclobutanones) in one single protocol.

Modification of Macroscopic Physico-Biological Parameters of the Food After being induced in the food matrix, some stable radiolytic products may change macroscopic physico-biological parameters of the food.

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Figure 6.6. Chromatogram of 2-alkylcyclobutanones extracted from 5 kGy irradiated milk powder (2-HCB induced from capric acid, 2-OCB induced from lauric acid, 2-DCB induced from myristic acid, 2-dDCB induced from palmitic acid, and 2-tDCB induced from stearic acid).

Gas Evolution A very simple method for the detection of irradiated dry and frozen foods was proposed by Furuta and others (1995) and improved by Roberts and others (1996) and by Delincée (1996). It consists of the release by fast heating of low-molecular gases produced on irradiating food components (lipid, water, protein, sugars, and so on) and trapped in the matrix of the dry or frozen food.These gases (H2, CO, H2S, NH3) can be very easily detected by multiple gas sensors even several months (dry grains) or years (frozen food) after the treatment. Unfortunately, this method was not used by other scientific teams and has never been validated. Cellular Wall Modifications Radiolytic products induced by radiation treatment may modify the physical properties of the food subjected to a radiation process.The electric impedance of fish (Ehlermann 1972) and potatoes (Hayashi and others 1993) may be modified after irradiation and was proposed as a test for food irradiation detection. However, it was shown by these authors that the measurements were not reliable because the variations of impedance, measured from one food to another, were more important than those that were due to the radiation process itself. Other physical properties of foods, such as their viscosity, capacity to rehydrate (dehydrated spices), membrane permeability, melting point, and so on, were also studied but unfortunately without any real success. Once again, the variability of the results due to the food itself (variety, origin, conservation, physical state, and so on) was always higher than the modifications induced by the radiation treatment of the food.

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Bacteriological Modifications Generally, the objective of radiation processing is the lowering of bacterial bioburden and the elimination of pathogenic flora. It was thus to be expected that scientists proposed microbiological methods to detect irradiated food. Two of these methods were subjected to interlaboratory analyses and standardized by the CEN (Anonymous 2000d, 2004). After a radiation treatment, the dead bacteria can still be detected either by microscopic fluorescence observation (Direct Epifluorescence Filter Technique or DEFT) or by immunological analysis of the endotoxins contained in the Gram negative bacteria (Limulus Amoebocyte Lysate test or LAL), whereas the viable bacteria can be enumerated by an Aerobic Plate Count (respectively APC or GNB). The total number of dead and viable microorganisms, including nonviable cells (very often higher than 104CFU.g–1), is compared with the number of viable microorganisms (very weak after an radiation treatment).When the difference between the total number of microorganisms (viable and nonviable) and the number of viable microorganisms is above or about 3 to 4 log units, the sample may be identified as having been irradiated. Of course, this method is not radiation specific, because the same result may be obtained after heating, fumigation or use of bactericidal agents. However, it allows a cheap and quick screening of food likely to be irradiated. Germination Inhibition Last, the radiolytic products can have consequences that are easy to detect on the evolution of food. It is well-known that the radiation treatments are used to inhibit germination of the bulbs and tubers. Kawamura and others (1996a) proposed a test for the detection of irradiated citrus fruits based on the germination inhibition of their seeds. This simple method (but very long because four days are necessary for the seed to germinate) was validated by an interlaboratory test (Kawamura and others 1996b) but never standardized, and then never used by the official food control laboratories.

Irradiated Ingredients and Low-Dose Irradiated Plants The European Directive 1999/2/EC (Anonymous 1999) makes it mandatory in all EU Member States to mention on the labels whether a food has been irradiated or contains irradiated ingredients irrespective of the in-

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clusion rate.The detection of irradiated foods, when sold as items, does not pose any major analytical problems because 10 standardized protocols have been published by CEN.The situation is not the same when the detection of an irradiated ingredient included in low amounts in a nonirradiated food is to be considered.The radiolytic products will be diluted to such low concentrations in the food matrix that they will not be detectable anymore because of the insufficient sensitivity and specificity of the currently available detection methods. Ndiaye and others (1999b) proposed the use of silver chromatography to enhance the selectivity and the sensitivity of the 2-alkylcyclobutanone method. Horvatovich and others (2002) proposed a modified highly sensitive SFE method. Both improvements allowed the detection of irradiated, mechanically recovered poultry meat in precooked meals, but also of a very low dose (0.05 to 0.1 kGy) treatment for insect disinfestation of cereals and leguminous plants (rice, avocados, cowpeas). Marchioni and others (2003) proposed an enzymatic hydrolysis, carried out at 55° C, for the extraction of silicate minerals and bone fragments present in precooked meals and cheeses containing very low levels of irradiated spices and/or mechanically recovered poultry meats (MRM) or fish.When followed by a purification of the extracts using an aqueous solution of sodium polytungstate, the extraction method made it possible to detect very low inclusions of irradiated spices (0.05% wt:wt by thermoluminescence) or irradiated MRM (0.5% wt:wt by ESR) included in various meals (cheeses and precooked meals). Even for food containing the two ingredients, it was possible to detect and identify them simultaneously.

Conclusion It is thus clear that detection of irradiated food (regarded as extremely difficult 10 years ago) is now possible thanks to standardized analytical methods used in food-control laboratories. The six reference methods adopted by the European Committee for Standardization allow the detection of the radiation treatment in the majority of foods likely to be irradiated. The four other methods (also adopted by the European Committee for Standardization), simple to implement and inexpensive, but whose applicability is restricted and specificity is lower, are used as screening methods. However, in spite of the 5,000 food samples analyzed in 2002 within the Northern Europe food control laboratories, only 2.7% were detected as not correctly labelled (1.4% if dietary supplements are excuded). Therefore, one could question the usefulness of the analytical, human,

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and financial efforts to set up protocols for food irradiation detection, and therefore for the control of food treated by a technology that poses only very few risks but numerous benefits for human health. References Anonymous. 1996a. Foodstuffs. Detection of irradiated food containing fat. Gas chromatographic analysis of hydrocarbons. EN 1784. Brussels (Belgium): European Committee for Standardization. 22 p. Anonymous. 1996b. Foodstuffs. Detection of irradiated food containing fat. Gas chromatographic/Mass spectrometric analysis of 2-alkylcyclobutanones. EN 1785. Brussels (Belgium): European Committee for Standardization. 14 p. Anonymous. 1996c. Foodstuffs. Detection of irradiated food containing bone. Method by ESR spectroscopy. EN 1786. Brussels (Belgium): European Committee for Standardization. 12 p. Anonymous. 1996d. Foodstuffs. Detection of irradiated food containing cellulose by ESR spectroscopy. EN 1787. Brussels (Belgium): European Committee for Standardization. 11 p. Anonymous. 1996e. Foodstuffs. Detection of irradiated food from which silicate minerals can be isolated. Method by thermoluminescence. EN 1788. Brussels (Belgium): European Committee for Standardization. 20 p. Anonymous. 1999. Directive 1999/2/EC of the European Parliament and of the Council of 22 February 1999 on the approximation of the laws of the Member States concerning foods and food ingredients treated with ionizing radiation. L66/16. Brussels (Belgium): The Official Journal of the European Communities 13 March 1999. p 16–25. Anonymous. 2000a. Foodstuffs. Detection of irradiated food containing crystalline sugar by ESR spectroscopy. EN 13708. Brussels (Belgium): European Committee for Standardization. 9 p. Anonymous. 2000b. Foodstuffs. Detection of irradiated food using photostimulated luminescence. EN 13751. Brussels (Belgium): European Committee for Standardization. 12 p. Anonymous. 2000c. Foodstuffs. DNA comet assay for the detection of irradiated foodstuffs—Screening method. EN 13784. Brussels (Belgium): European Committee for Standardization. 17 p. Anonymous. 2000d. Foodstuffs. Detection of irradiated food using Direct Epifluorescence Filter Technique/Aerobic Plate Count (DEFT/APC)—Screening method. EN 13783. Brussels (Belgium): European Committee for Standardization. 17 p. Anonymous. 2004. Foodstuffs. Microbiological screening method for irradiated food using LAL/GNB procedures. EN 14569. Brussels (Belgium): European Committee for Standardization. 16 p. Bacquet G,Truong VQ,Vignoles M,Trombe JC, Bonel G. 1981. ESR of carbon dioxide radical anion in x-irradiated tooth enamel and A-type carbonated apatite. Calcif Tissue Int. 33:105–109. Bögl KW, Heide L. 1985. Chemiluminescence measurements as an identification method for gamma-irradiated foodstuffs. Radiat Phys Chem. 25:173–185. Deighton N, Glidewell SM, Goodmann BA, Morisson IM. 1993. Electron paramagnetic resonance of gamma-irradiated cellulose and lignocellulosic material. Int J Food Sci Technol. 28:45–55.

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Delincée H. 1987. Ist die Bestrahlung von Gewürzen durch Chemiluminescenz nachweisbar? Fleischwirtschaft. 67:1410–1418. Delincée H, Ehlermann DAE. 1989. Recent advances in the identification of irradiated food. Radiat Phys Chem. 34:877–890. Delincée H. 1991.Analytical detection methods for irradiated foods—a review of the current literature, IAEA Tecdoc 587.Vienna (Austria): IAEA. 172 p. Delincée H. 1996.A rapid and simple screening test to identify irradiated food using multiple gas sensors. In: McMurray CH, Stewart EM, Gray R, Pearce J, Editors. Detection Methods for Irradiated Foods—Current Status. Cambridge (United Kingdom):The Royal Society of Chemistry. p. 326–330. Delincée H, Soika C. 2002. Improvement of the ESR detection of irradiated food containing cellulose employing a simple extraction method. Radiat Phys Chem 63:437–441. Ehlermann DAE. 1972. The possible identification of an irradiation treatment of fish by means of electrical (ac) resistance measurement. J Food Sci 37:501. Farkas J, Koncz A, Sharif MM. 1990. Identification of irradiated dry ingredients on the basis of starch damage. Radiat Phys Chem 35:324–328. Furuta M, Dohmaru T, Katayama T, Toratani H, Takeda A. 1995. Retention of radiolytic CO gas in irradiated pepper grains and irradiation detection of spices and dry grains with the level of stocked gas. J Agric Food Chem 43:2130–2133. Hart RJ,White JA, Reid WJ. 1988. Occurrence of o-tyrosine in nonirradiated foods. Int J Food Sci Technol 23:643–647. Hasselmann C, Laustriat G. 1973. Photochimie des acides aminés aromatiques en solution—I. DL-Phenylalanine, DL-Tyrosine et L-Dopa. Photochem Photobiol 17:275–294. Hasselmann C, Grimm L, Saint-Lèbe L. 1986. Mise en évidence de l’irradiation des aliments par des méthodes physico-chimiques. Med Nut 22:121–126. Hasselmann C, Marchioni E. 1991. Physicochemical methods for the detection of food irradiation. In: S Thorne, ed. Food Irradiation.Amsterdam (The Netherlands): Elsevier Appl Sci 129–168. Hayashi T,Todoriki S, Otobe K. 1993.Applicability of impedance measuring method to the detection of irradiated treatment of potatoes. Nippon Shokuhin Kogyo Gakkaishi 40: 378–384. Hein WG, Simat TJ, Steinhart H. 1999. Nachweis der ␥-Bestrahlung von Nordseegarnelen über nicht proteingebundenes o-Tyrosin. In Knörr M, Ehlermann DAE, Delincée H, Eds. Lebensmittelbestrahlung -5. Deutsche Tagung-. Karlsruhe (Germany): Berichte der Bundesforshunganstahlt für Ernährung. BFE-R-99-01. p. 148–152. Horvatovich P, Miesch M, Hasselmann C, Marchioni E. 2000. Supercritical fluid extraction of hydrocarbons and 2-alkylcyclobutanones for the detection of irradiated foodstuffs. J Chromatogr A 897:259–268. Horvatovich P, Miesch M, Hasselmann C, Marchioni E. 2002. Supercritical fluid extraction for the detection of 2-dodecylcyclobutanone in low dose irradiated plant foods. J Chromatogr A 968:251–255. deJesus EFO, Rossi AM, Lopes RT. 1996. Influence of sample treatment on ESR signal of irradiated citrus.Appl Radiat Isot 47:1647–1653. deJesus EFO, Rossi AM, Lopes RT. 1999.An ESR study on identification of gamma-irradiated kiwi, papaya and tomato using fruit pulp. Int J Food Sci Technol 34:173–178. Kawamura Y, Murayama M, Uchiyama S, Saito Y. 1996a. Development of half-embryo test and germination test for detection of irradiated fruits and grains. In: McMurray CH, Stewart EM, Gray R, Pearce J, Eds. Detection Methods for Irradiated Foods—Current Status. Cambridge (United Kingdom):The Royal Society of Chemistry. p. 383–391.

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Kawamura Y, Sugita T,Yamada T, Saito Y. 1996b. Half-embryo test for identification of irradiated citrus fruit: collaborative study. Radiat Phys Chem 48:665–668. Marchioni E,Tousch M, Zumsteeg V, Kuntz F, Hasselmann C. 1992.Alterations of mitochondrial DNA: A method for the detection of irradiated beef liver. Radiat Phys Chem 40:485–488. Marchioni E, Horvatovich P, Ndiaye B, Miesch M, Hasselmann C. 2003. Detection of low amount of irradiated ingredients in non-irradiated precooked meals. Radiat Phys Chem 63:447–450. McMurray CH, Stewart EM, Gray R, Pearce J. 1996. Detection Methods for Irradiated Foods—Current Status. Cambridge (United Kingdom):The Royal Society of Chemistry. 431 p. Nawar WW. 1986.Volatiles from food irradiation. Food Rev Int 21:45–78. Nawar WW. 1994. Progress in the detection of irradiated foods by measurement of lipidderived volatiles. In: McMurray CH, Stewart EM, Gray R, Pearce J, Eds. Detection Methods for Irradiated Foods—Current Status. Cambridge (United Kingdom):The Royal Society of Chemistry. p 241–248. Ndiaye B, Jamet G, Miesch M, Hasselmann C, Marchioni E. 1999a. 2-Alkylcyclobutanones as markers for irradiated foodstuffs. II.The CEN (European Committee for Standardization) method: Field of application and limit of utilization. Radiat Phys Chem 55:437–445. Ndiaye B, Horvatovich P,Miesch M,Hasselmann C,Marchioni E.1999b.2-Alkylcyclobutanones as markers for irradiated foodstuffs: III. Improvement of the field of application on the EN 1785 method by using silver ion chromatography. J Chromatogr A 858:109–115. Östling O. 1988. Radiation induced DNA strand breaks in single cells. In: Bögl KW, Regulla DF, Suess MJ, Editors. Health Impact, Identification, and Dosimetry of Irradiated Foods, Report of a WHO working group. ISH 125. Neuherberg (Germany): Bundesgesundheitsamt. P. 305–307. Pfeilsticker K, Lucas J. 1987. Die fluorimetrische Bestimmung von Thyminglycol in Lebensmitteln (biologischem Material)—der Thyminglycolgehalt als Kriterium für eine Behandlung mit ionisierenden Strahlen.Angew Chem 99:341–342. Raffi J,Agnel JP. 1989. Electron spin resonance identification of irradiated fruits. Radiat Phys Chem 34:891–894. Raffi J, Stevenson MH, Kent M,Thiery JM, Belliardo JJ. 1992. European intercomparison on electron spin resonance identification of irradiated foodstuffs. Int J Food Sci Technol 27:111–124. Raffi J, Delincée H, Marchioni E, Hasselmann C, Sjöberg AM, Leonardi M, Kent M, Bögl KW, Schreiber G, Stevenson H, Meier W. 1993. Concerted action of the Community Bureau of Reference on the Methods of Identification of Irradiated Foods, EUR 15261 EN, Brussels (Belgium): BCR. 119 p. Roberts PB, Chambers DM, Brailsford GW. 1996. Gas evolution as a rapid screening method for detection of irradiated foods. In: McMurray CH, Stewart EM, Gray R, Pearce J, Eds. Detection Methods for Irradiated Foods—Current Status. Cambridge (United Kingdom):The Royal Society of Chemistry. p 331–334. Rossi AM,Wafcheck CC, de Jesus EF, Pelegrini F. 2000. Electron spin resonance dosimetry of teeth of Goiânia radiation accident victims.Appl Radiat Isot 52:1297–1303. Sanderson DCW, Slater C, Cairns KJ. 1989.Thermoluminescence of foods: Origins and implications for detecting irradiation. Radiat Phys Chem 34:915–924. Sanderson DCW, Carmichael LA, Spencer JQ, Naylor JD. 1996. Luminescence detection of shellfish. In: McMurray CH, Stewart EM, Gray R, Pearce J, Eds. Detection Methods for Irradiated Foods—Current Status. Cambridge (United Kingdom): The Royal Society of Chemistry. P. 139–148.

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Simic MG, Dizdaroglu M, DeGraff E. 1983. Radiation chemistry. Extravaganza or an integral component of radiation processing of food. Radiat Phys Chem 22:233–239. Soika C, Delincée H. 2000.Thermoluminescence analysis for detection of irradiated food— Luminescence characteristics of minerals for different type of radiation and radiation doses. Lebensm-Wiss u-Technol 33:431–439. Stevenson MH, Crone AVJ, Hamilton JTG. 1990. Irradiation detection. Nature 344:202–203. Swallow AJ. 1988. Some approaches based on radiation chemistry for identifying irradiated food. In: Bögl KW, Regulla DF, Suess MJ, Eds. Health Impact, Identification, and Dosimetry of Irradiated Foods, Report of a WHO working group. ISH 125. Neuherberg (Germany): Bundesgesundheitsamt. P. 128–138. Tabner BJ, Tabner VA. 1994. Electron spin resonance spectra of ␥-irradiated citrus fruits skins, skin components and stalks. Int J Food Sci Technol 29:143–152. Takano M, Fukao Y. 1994. ESR dating of Pleistocene fossil shells of the Atsumi group, Central Honshu, Japan: On the discrepancy in TD value among different ESR peaks.Appl Radiat Isot 45:49–56. VonSonntag C. 1987.The Chemical Basis of Radiation Biology. London (United Kingdom): Taylor and Francis. 515 p. Tyreman AL, Bonwick GA, Smith CJ, Coleman RC, Beaumont PC, Williams JHH. 2004. Detection of irradiated food by immunoassay-development and optimisation of an ELISA for dihydrothymidine in irradiated prawns. Int J Food Sci Technol 39:533–540. Williams JHH, Tyreman AL, Deeble DJ, Jones M, Smith CJ, Christiansen JF, Beaumont PC. 1994. Immunochemical detection of modified DNA bases in irradiated food. In: McMurray CH, Stewart EM, Gray R, Pearce J, Eds. Detection Methods for Irradiated Foods—Current Status. Cambridge (United Kingdom):The Royal Society of Chemistry. P. 367–374.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 7 DOSIMETRY FOR FOOD PROCESSING AND RESEARCH APPLICATIONS Kishor Mehta, Ph.D., and Kevin O’Hara

Importance of Dosimetry Food products may be treated with ionizing radiation for various purposes including insect disinfestation, growth inhibition, control of parasites, and shelf-life extension. Food irradiation specifications usually include an upper-dose limit to avoid product and product packaging degradation and lower-dose limit to ensure the intended beneficial effect. For food processing, the upper-dose limit is set for good irradiation practice and not from a food safety viewpoint (IAEA 2002). Much research and experimentation are carried out to set these dose limits suitable for the food product and the process under consideration. Due to the farreaching influence of the outcome of these experiments, it is imperative that the dose measurements are very accurate to arrive at a reliable set of dose limits for the process (ISO/ASTM 2004a).These dose limits are then often prescribed by regulations, where again proper dosimetry helps to verify compliance with these regulations at a commercial facility, as well as with national and international standards. Dosimetry is an integral part of both research and radiation-processing applications. It is important, therefore, that dosimetry personnel have some basic understanding of the radiation physics and chemistry of dosimetry.This chapter deals mainly with the application of dosimetry in food processing (for both commercial processing and radiation research); for those who are interested, references to the chemistry and physics of radiation dosimetry are given throughout the chapter. As a minimum requirement, food-processing personnel involved with dosimetry should have relevant experience and training.

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There are fundamental requirements for dosimetry in the process of conducting research on the irradiation of food and agricultural products that are based on good scientific practices. Radiation research for food often involves the establishment of the quantitative relationship between the absorbed dose and the relevant radiation-induced effects in these products.This effect in the food product is often measured with state-ofthe-art analytical equipment, but the absorbed dose to induce that effect is sometimes treated with less importance.The measurement and reporting of absorbed dose should be treated with equal importance, as with the measurement of these effects.

Introduction Proper dosimetry depends on the user’s ability to measure the absorbed dose to the food product, on the ability to determine the absorbed-dose distribution throughout the food product, and on the ability to perform routine dosimetry during processing or research. In the case of research, the delivery of the desired absorbed dose to the food product under known and validated conditions also requires good dosimetry.The accurate measurement of the dose distribution gives confidence that the maximum absorbed dose (Dmax) and minimum absorbed dose (Dmin) have indeed been measured. The principal objective of dosimetry in research is the determination of dose to achieve a desired effect. However, it is also necessary to establish baseline data in experimental design and to determine the dose distribution in the research sample. Because absorbed dose is the quantity that relates directly to the radiation-induced effect, the need for accurate dose measurement cannot be overestimated. In radiation processing, the overexposure or underexposure of the food product may have economic and legal consequences. In radiation research, the consequence is that incorrect conclusions are reached. Radiation-processing applications include operational qualification (such as irradiator dose mapping), process qualification (such as product dose mapping) and routine process control (such as routine product dosimetry for product release). For both research and radiation-processing applications, dosimetry measurements should be part of an overall quality assurance program. The dosimetry procedures should be based on internationally recognized practices such as those of International Organization for Standardization (ISO), European Committee for Standardization (CEN), and American Society for Testing and Materials, International (ASTM).

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Some Fundamentals of Dosimetry The measurement of absorbed dose involves a chemical or physical dosimeter whose well-defined and established radiation-induced effect is measured (for example, by spectrometers or spectrophotometers) and related to absorbed dose via the dosimetry system’s calibration curve. Several types of dosimetry systems are used in food irradiation (for example, liquids, plastic, radiochromic or alanine films, or pellets). For all of the dosimetry systems mentioned in this chapter, ISO/ASTM standards exist on their use; in addition, ISO/ASTM gives guidance on the selection and calibration of an appropriate dosimetry system (ISO/ASTM 2004b). Absorbed Dose In the irradiation of food products for processing or research, the emphasis is on “absorbed dose”and is defined as the quantity of ionizing radiation energy imparted per unit mass of a specified material. The SI unit of absorbed dose is the gray (Gy), where 1 Gy equals 1 J/kg.The absorbed-dose range of interest in food irradiation varies significantly and is generally categorized as low, medium, and high as defined in Table 7.1 (IAEA 2002). For food irradiation applications, water is usually considered the reference material and dose generally refers to “dose to water.” The vast majority of dosimeters available for food applications are considered waterequivalent in composition (for example, polymethylmethacrylate [PMMA] and radiochromic film). Dosimetry System A dosimetry system is used for determining absorbed dose and consists of dosimeters, measurement instruments, and procedures for the system’s use.A dosimeter is a device that, when irradiated, exhibits a quantifiable change in some property that can be related to absorbed dose using measurement instrumentation. In addition, reference standards are often considered to be part of a dosimetry system. These reference standards could include absorbance and wavelength standards for instrument calibration or instrument performance checks. Selection and Characterization of a Dosimetry System Types of Dosimetry Systems Dosimetry systems are classified based on their intrinsic accuracy and applications into one of four categories: primary-standard dosimeters,

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Table 7.1. Low, Medium, and High Dose Ranges for Food Processing and Research (IAEA 2002) Dose Range (Low, Medium, or High) Low Low Low

Low Low Medium Medium

High

High

Irradiation Application Sprout inhibition (for example, potatoes, onions, garlic, yams) Delay in ripening (for example, strawberries, potatoes) Insect disinfestation (for example, insects in grains, cereals, coffee beans, spices, dried fruits, dried nuts, dried fish products, mangoes and papayas) Quarantine security (against, for example, tephretid fruit flies in fruits and vegetables) Inactivation of pathogenic parasites (for example, tape worm and trichina in meat) Reduction in food spoilage causing microorganisms Improve the hygienic quality of food by inactivating foodborne pathogenic bacteria and parasites Pathogenic organism reduction in dried spices, herbs and other dried vegetable seasonings Sterilization to extend the shelf life of precooked food products in hermetically sealed containers

Typical Dose or Dose Range (Gy) 20 to 150 10 to 1,000 20 to 1,000

150 300 to 1,000 1,000 to 10,000 1,000 to 8,000

10,000 to 30,000

25,000 to 75,000

reference-standard dosimeters, transfer-standard dosimeters, and routine (or working) dosimeters (ISO/ASTM 2004b). Primary-standard dosimeters enable an absolute measurement of absorbed dose and are maintained and operated by national laboratories (for example, NIST and NPL). There are two types of primary-standard dosimeters: ionization chambers and calorimeters (ISO/ASTM 2004b). Reference-standard dosimeters are dosimeters of high metrological quality that can be used as reference standards to calibrate other dosimeters. They must have a radiation response that is accurately measurable and has a well-defined relationship with the dose. Commonly used reference-standard dosimeters include Fricke, ceric-cerous, dichromate, ethanol-chlorobenzene (ECB), and alanine dosimeters (ISO/ASTM 2004b). Transfer-standard dosimeters are used for transferring dose informa-

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tion from an accredited laboratory to an irradiation facility or a research laboratory.These dosimeters are normally reference-standard dosimeters that have characteristics meeting the requirements of the particular application. For example, they have to be transported from one place to another; there is also a time delay between the irradiation and their analysis (ISO/ASTM 2004b). Routine (or working) dosimeters are used for dose mapping and for process monitoring for quality control.They are often calibrated against reference- or transfer-standard dosimeters.Alternatively, the calibration of the routine dosimeter should be verified under actual conditions of use using a reference- or transfer-standard dosimeter. Commonly used routine dosimeters include PMMA and radiochromic dosimeters (ISO/ASTM 2004b). The Selection of an Appropriate Dosimeter As mentioned earlier, dosimetry is an essential part of radiation processing, especially for achieving a reliable process and thus a quality end product. A dosimetry system should be carefully selected in the early planning stages of the irradiation project. Selection is based on understanding the dosimetry requirements of the process and matching them to the characteristics of the dosimetry system.A dosimetry system for research applications may be different than the system that is suitable for commercial processing. The criteria for selection of a suitable dosimeter (and dosimetry system) may differ between a routine dosimeter and reference-standard dosimeter and are technical or operational in nature.The following list of criteria is not exhaustive, but examples are given to illustrate why certain attributes are important (ISO/ASTM 2004b and IAEA 2002). Suitable dose range for the applications: Food irradiation dose ranges vary from low dose levels (10 Gy to 1 kGy) to medium dose levels (1 kGy to 10 kGy) to high dose levels (10 kGy to 100 kGy).The user may wish to use one dosimeter to span the entire range of applications, but doing so may not be possible. More than one system may be required at the facility. Figure 7.1 gives the useful dose ranges for a number of common dosimetry systems suitable for food irradiation (ISO/ASTM 2004b and IAEA 2002). Post-irradiation change in dosimeter response: The time required for dosimeter’s response to develop following irradiation will vary from dosimeter type to dosimeter type. In the case in which irradiated product is released for use based on dosimetry results, this may be very important, but for some research applications may not be important.

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Figure 7.1.

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Useful dose range for various dosimeters (ISO ASTM/2004b).

Ruggedness of the dosimeter: For example, resistance to damage during normal routine handling could be critical. Many dosimeters may be supplied in a protective cover. Ease of system use: The form of a dosimeter ranges from a thin film, to a glass ampoule, to a pellet, to an optically transparent piece, and differs considerably in the method of handling, readout and general use. Stability of dosimeter response both before and after irradiation is important, as well as the ability to correct for influence quantities. In addition, the readout methods vary from UV/visible spectrophotometry to EPR spectroscopy to potentiometric techniques.All dosimetry systems require good laboratory practice, but ease of use should be considered. Capital investment: Initial capital investment and ongoing operational cost of the system, including dosimeters, measurement instruments, and labor, will vary from system to system. Dose mapping: The size of the dosimeter and its ability to measure dose gradients are important considerations. Significant dose gradients will likely exist at the interface between materials of different density (for example, near the bone-tissue interface in the cavity of a chicken or near the surface of a nectarine pit). It is important to use dosimeters that are capable of measuring these variations. For example, a film dosimeter is small relative to distances over which the dose gradient is significant.

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Type of irradiation facility and source: Different types of irradiation facilities may produce gamma rays, electrons or x-radiation (bremsstrahlung) with energies ranging from 0.1 MeV to 10 MeV. Some dosimetry systems may not be suitable for electrons and photons or low-energy radiation. Dosimetry System Characterization Before a dosimetry system is used, it should be characterized.The characterization consists of calibration, estimate of overall uncertainty, determination of batch homogeneity, establishment of traceability, and understanding of the effect of influence quantities on the dosimeter’s response. Similar to any other measurement system, a dosimetry system must be calibrated before being used.Three methods of dosimetry system calibration are described in detail in ISO/ASTM 51261 (2004b) and NPL Report CIRM 29 (1999). Uncertainty in the measured absorbed dose will differ significantly among dosimetry systems. Indeed, the knowledge about desired level of overall (or total) uncertainty for a specific food application will help to select an appropriate dosimetry system for that application. ISO/ASTM Guide 51707 (2004c) and NPL Report CIRM 29 (1999) describe possible sources of uncertainty in dosimetry and offer procedures for estimating the uncertainties. Regardless of the application (research or commercial), an estimate of uncertainty should accompany the measured and reported dose value (Mehta 2002).Typically, overall uncertainty in dose for reference-standard dosimeters should be better than 5% (at the 95% confidence level) and for routine dosimeters should be better than 8% (at the 95% confidence level). ISO/ASTM Guide 51707 (2004c) uses an uncertainty methodology adopted by ISO in 1995, which is different from the way uncertainty has been traditionally expressed in terms of “precision” and “bias.” Batch homogeneity represents the extent of variability of the dosimeter’s response for a given batch of dosimeters. How well does a calibration accurately represent the dosimetry system, including the entire batch of dosimeters? An indication of batch homogeneity is derived during the dosimetry system calibration.The procedure for estimating batch homogeneity is described in IAEA 2002. A measured dose value is called traceable when it can be related to recognized standards, usually national or international standards within acceptable limits. Traceability is a prerequisite for radiation-processing dosimetry and is also recommended for food research dosimetry (IAEA 2002).

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The reality of absorbed dose measurement is that the response of the dosimeter is affected by influence quantities that may not be within the control of the food processing or research facility. Such influence quantities include irradiation and storage temperature of dosimeters, dosimeter humidity, absorbed-dose rate, and radiation energy spectrum. It is important to understand how these influence quantities affect the response of the dosimeters, as well as the interpretation of dose and the estimate of uncertainty (ISO/ASTM 2004c). The effects of influence quantities may introduce significant uncertainties if the conditions during calibration differ from those during routine use.These effects must be evaluated.

The Use of a Dosimetry System Numerous ISO/ASTM standard practices and guidelines have been written on the use of specific dosimetry systems.These standards include the recommended instrumentation performance check, calibration techniques (including irradiation), storage and handling guidelines, dosimeter analysis techniques, dosimeter characterization (including postirradiation characterization), and documentation requirements. Another important consideration in the use of a dosimetry system is that, ideally, the presence of the dosimeter does not appreciably disturb the photon and electron energy spectrum in the volume where the dosimeter is located. Ideally, the dosimeter’s effective atomic number is similar to that of the irradiated material. For dose measurement in a hydrogenous material (for example, fruit, meat, poultry, or vegetable), a dosimeter of low-atomic number is useful (for example, aqueous solutions, PMMA, radiochromic thin film, alanine).

Dosimetry in Food Research Research on the effectiveness of irradiation of food products to achieve a defined benefit may involve different experimental parameters from one test to another. For example, the dose necessary for fruit disinfestation is much lower than the dose required for the bacterial inactivation in meat. In addition, the type of irradiation source may be different from facility to facility.The radiation-induced effect may also depend on other factors, for example, the absorbed-dose rate and energy of the radiation. Indeed, the radiation-induced effect may be different for two specimens that received the same absorbed dose but under different conditions.The radiation-induced effect in the food product depends on a large number

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of factors that may be physical, physiological, or chemical. Also, several environmental factors (for example, irradiation and analysis temperature of dosimeters, and moisture content in the food) may affect the radiation response of dosimeters; these should be documented. In research, an experiment is often designed to irradiate the specimen uniformly, but in practice, a variation in absorbed dose will exist throughout the specimen. Absorbed-dose mapping is performed to determine this variability—for example, the magnitude and location of Dmax and Dmin for a set of defined experimental parameters. One of the principal objectives in experimental design is to establish baseline data for evaluating the effectiveness and reproducibility of the experiment. Dosimetry is part of this experimental design. Proper dosimetry will allow the researcher to differentiate absorbed-dose variations that are expected under normal experimental conditions. Most important, dosimetry allows the researcher to measure absorbed-dose distributions in the irradiated specimen and to associate the absorbed dose with the radiation-induced effect. Documented experimental procedures ensure a reproducible dose distribution in the irradiated food, and allow other scientists to repeat the experiment. In research, dose mapping may involve the measurement of absorbeddose distribution through a single fruit, or box of fruit. This is achieved by placing dosimeters throughout the volume of interest, including the surface and within the volume. Even if the researcher is certain of the resultant dose distribution, the initial experiments should consist of a very thorough placement of dosimeters. Data from previous experiments can provide useful information for determining the number and location for these dosimeters.After the distribution is accurately determined, including the reproducibility of the measurements, dosimeter placement at and near zones of Dmax and Dmin is warranted for subsequent irradiations. In some applications, the irradiated food product may experience pronounced dose gradients on the surface or within the volume. Smalldimension dosimeters (for example, radiochromic film) may be used to measure these gradients. In the case when there is a large difference between dose extremes, it may be difficult to associate an absorbeddose level with an induced effect, unless that induced effect is relatively constant. A number of factors will affect the absorbed-dose distribution: sourceto-product distance; primary radiation scattered from experimental apparatus into the volume of interest; composition of the product packaging; and containment. Experimental set-ups that yield complex dose distributions or significant dose variation should be avoided. After the absorbed-dose distribution has been established for a given

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experimental set-up, the routine measurement of absorbed dose continues (ISO/ASTM 2004a).This measurement is often at a reference-dose location and does not require continued extensive dosimetry unless experimental conditions are changed with a resultant change in the dose distribution. Changes that could impact the dose distribution include changes in the radiation source or a significant alteration in the food geometry or packaging material. Theoretical calculations may also be used to determine absorbed-dose distribution in the irradiated food, and complement absorbed-dose measurement (ASTM 2004a). Calculations may also be used to evaluate the impact of changes in the experimental set-up, and to help optimize the set-up.

Dosimetry at a Commercial Facility General The dosimetry system selected for research may not be necessarily most suitable at the commercial facility.Thus it may be necessary to go through the selection process based on the criteria listed earlier. A second measurement instrument as a back-up is recommended for the selected routine dosimetry system. Some large irradiation facilities also have a referencestandard dosimetry system. Dosimetry plays a key role for two major activities at a commercial facility: • process validation, which includes characterization and maintenance of the irradiator, and the radiation process itself, and • routine process control, which includes those activities that control the process during routine operation and that gather evidence/information to show that this routine operation was under control. Process Validation Process validation is used to show that the entire process is under control.This involves establishing documented evidence that provides a high degree of assurance that a specific process will consistently produce a product that meets its predetermined specifications and quality characteristics.The best and most convenient method of documenting such evidence is through reliable dosimetry. The framework of such a process validation program includes:

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• operational qualification • process qualification Each of these activities is briefly described below, including the demands each puts on the dosimetry system. It is essential that validation is maintained through relevant activities carried out at regular intervals. Operational Qualification The commissioning and the subsequent operational qualification are the responsibility of the facility owner/operator. Operational qualification includes testing, calibrating, and characterizing the equipment at the facility, including the source and its ancillary control system, the conveyor system, any weighing equipment, and the dosimetry system(s) in use at the facility.These tasks are carried out after the commissioning of the facility and are repeated at regular intervals and whenever changes are introduced that may significantly affect dose or dose distribution in the irradiated products. Dosimetry is an important element in qualifying an irradiation facility, especially in establishing baseline data for evaluating facility effectiveness, predictability, and reproducibility for the range of conditions of operation. For example, dosimetry is used: • for irradiator dose mapping (measuring absorbed-dose distributions in reference materials with reference irradiation geometry) • for characterizing the facility, including establishing relationships between absorbed dose and operating parameters of the facility These procedures are described in ISO/ASTM Practice 51204 (2004d) for gamma-ray facilities and in ISO/ASTM Practice 51431 (2004e) for electron and x-ray facilities.These activities are also described briefly here. Irradiator Dose Mapping In a commercial irradiation facility, product may be transported through the radiation field using different methods (for example, tote box, carrier, or on a pallet). For simplicity in the following discussion, this method is referred to as a carrier. To determine the capability of an irradiator, it is important to locate the regions of Dmax and Dmin and their values within such a carrier, which is achieved by measuring a threedimensional dose distribution (dose mapping) in a carrier filled with a homogeneous reference material.For this purpose, a reference material may be selected that has composition and density close to food product

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that would be irradiated at the facility. Options are bulk feed ingredients that are relatively inexpensive; for example, rolled barley (density ~ 0.4 g/cm3), dehydrated alfalfa (~ 0.5 g/cm3), and whole corn (~ 0.7 g/cm3). Such dose mapping requires placing a sufficient number of dosimeters throughout the carrier in a systematic grid form; however, placing more dosimeters in the region where dose is expected to be extreme, based on general knowledge or previous experience with similar irradiators or from theoretical calculations. Dosimeters should be selected depending on the irradiation geometry; the size of the dosimeters should be such that they can spatially resolve the dose variation expected in the carrier. For example, thin film dosimeters are essential for an electron facility because of high dose gradients. For dose mapping, precision is more important than accuracy, because only dose variation is required.Thus it may be necessary to choose a dosimetry system that is different from the one used for process control during routine production.An acceptable way to refer to the uniformity of dose in the carrier is “dose uniformity ratio, DUR,” defined as the ratio of Dmax and Dmin. Figure 7.2 shows a typical

Figure 7.2. An example of the Dmax and Dmin locations in product for a two-pass gamma ray facility (IAEA 2002).

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Figure 7.3. An example of the Dmax and Dmin locations in product for an electron beam irradiation facility after one pass (IAEA 2002).

irradiation geometry for a rectangular product carrier for a gamma-ray facility, where hatching indicates the probable regions of Dmax and Dmin after the second pass. Figure 7.3 shows a typical irradiation geometry for an electron facility, where hatching indicates the probable regions of Dmax and Dmin for a rectangular carrier following a one-sided irradiation. Characterization of the Facility An irradiation facility is thoroughly characterized before it is used for commercial purposes (Cavaco and others 1991; Kovács and others 1998). Characterization includes the determination of the relationships between absorbed dose (or dose rate) and those process parameters that affect the dose in the product, over the full operational range of the parameters. These parameters include source strength and source arrangement, conveyor speed or dwell time, multi-pass mode, irradiation geometry, and bulk density of product. For an accelerator facility (both for electron and x-ray mode), there are also other parameters that are important, such as electron beam current,beam energy,beam spot,and scan width and scan frequency. Gamma-ray facility: The dose delivered to the food product depends strongly on either the selected dwell time or conveyor speed, which is most frequently used to control dose to the product. Dose rate also depends on the bulk density of the product; to deliver the same dose to a

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product, it would take longer time as the bulk density increases.These relationships should be established during operational qualification; this understanding is of practical help for the operation of the facility, and especially during process qualification. For this purpose, real products or simulated products (such as reference materials) may be used.The bulk density of the simulated products should be chosen to cover a range of values that are expected to be irradiated at the facility.The dosimeters are placed, by preference, at locations where minimum dose is expected (as determined during irradiator dose mapping).The data should then be analyzed using regression analysis to obtain the relationships between the variables. Accelerator facility: Characterization of an accelerator irradiator would also include measuring the mean energy of the electron beam, beam spot profile, and scan width (ISO/ASTM 2004f); information about the last two parameters helps to assure that the dose is uniformly delivered on the surface of a product carrier. For these two parameters, it is very convenient to use a strip or a large sheet of dosimetric film material. The penetration of the electrons depends on the beam energy (and on the composition and density of the product); thus, the beam energy is practically measured by determining the variation of dose with depth (depth-dose distribution) along the beam axis in a reference material. Figure 7.4 shows a typical depth-dose distribution that is generally measured by exposing either several thin film dosimeters at different depths in stack geometry or a strip of dosimetric material in a wedge (ISO/ASTM 2004f).The reference material is generally low atomic number material, such as polystyrene, water, graphite, or aluminum.The range parameters, namely optimum thickness (Ropt), half-value depth (R50), and halfentrance depth (R50e), may be used for designing a suitable carrier, while parameters R50 and practical range (Rp) can be used for estimation of mean electron beam energy and the most probable electron beam energy based on mathematical relationships (ISO/ASTM 2004f; ICRU 1984). Process Qualification The goal of the irradiation process is to deliver dose to every part of the product that is between the two prescribed dose limits.These limits are established based on research results and are generally stipulated by regulators. The objective of process qualification is therefore to determine the values of all key process parameters (including timer setting, conveyor speed, and the characteristics of the product carrier, such as arrangement of product within) that will satisfy these dose specifications (and others, if any, such as temperature control for frozen food) with a

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Figure 7.4. Typical (idealized) depth-dose distribution for a 10MeV electron beam in homogeneous material composed of low-atomic number elements.The peak-to-surface dose ratio depends on the energy of the incident electron beam. For definitions of Ropt, R50, R50e, and Rp, refer to ISO/ASTM 51649 (2004f). Reprinted with permission of ISO/ASTM 2004f, copyright ISO/ASTM International.

high degree of confidence.This is achieved by measuring the dose distribution for the product in a specific product carrier with a specific product arrangement and is referred to as “product dose mapping.” Product Dose Mapping The objective of product dose mapping is to determine the locations and values of Dmax and Dmin in the carrier that is under consideration; these values are then compared against the dose limits. First, the detailed dose distribution is measured for one carrier—generally requiring 50 to 100 dosimeters depending on the degree of product homogeneity (Polonia and others 1998). For products with voids or nonuniform products (such as whole chicken), dosimeters should be placed at locations where discontinuities in composition or density may affect the regions of Dmax and Dmin (Miller and Batsberg 1981). Initially, the process parameters may be selected on a trial basis, based on past experience and operational

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qualification data. After irradiation, the dosimeters are removed, with careful noting of the position of each. The dosimeters are analyzed and the dose values determined. Dmax and Dmin are identified (ASTM 2004b) and the DUR value calculated.The objective is to achieve DUR value less than the ratio between the prescribed dose limits. If that is not the case, one or more process parameters need to be adjusted to decrease DUR following some of the methods described next. • For gamma-ray facilities: • extend the source beyond the boundaries of the product (source overlap) • move the carrier past the source at several different levels (product overlap) • use attenuators or compensating dummy • irradiate from two or four sides, or rotate the carrier during irradiation, and • increase the source-to-product distance • For electron facilities: • change the beam characteristics, for example, by optimizing the electron beam energy • use attenuators, scatterers, or reflectors • use double-sided irradiation depending on the bulk density, thickness, and heterogeneity of the product • arrange baffles to control product flow through the irradiation zone in the case of bulk-flow irradiators (for both types of facilities) If the DUR is still not acceptable, rearrangement of the product within the product carrier or alteration of its size may be necessary. Verification process The distribution of absorbed dose within the product depends on many factors, such as plant design, type of product, and energy and type of radiation. These factors will not normally vary during a given radiation process. However, due to the statistical nature of the radiation process, there are fluctuations in the values of some of the process parameters affecting the dose distribution (McLaughlin and others 1989; Biramontri and others 1989; Mehta 1992). In practice, variability is unavoidable in any radiation process due to several effects, including: • variation in the bulk density or product configuration between carriers • variation of dosimeters in placement, that is, dosimeters are not placed exactly at identical locations in different carriers

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• statistical fluctuations of some of the process parameters during irradiation • uncertainty associated with the dosimetry system The extent of this variability may be measured by randomly selecting a number of nominally identical carriers, n, where n is between 3 and 10. Several dosimeters are placed in each carrier in the expected zones of Dmax and Dmin, as identified during the product dose mapping exercise. These carriers are then irradiated together or sequentially, keeping all the process parameters nominally constant. Dmax and Dmin will vary due to the factors discussed above.These n values are expected to follow a normal (Gaussian) distribution characterized by two parameters, the mean value and the standard deviation. The standard deviations for Dmax and Dmin may not have the same value. These two standard deviations are then used to set “target doses” as discussed below.This exercise is sometimes referred to as “verification process.” Target Doses To ensure that the measured dose in the product during routine production is within the two specified dose limits in the presence of this variability, the operator sets the process parameters (such as dwell time or conveyor speed) so as to deliver a dose between two more restrictive limits.Thus, the lower dose limit is adjusted upward (higher value) while the upper dose limit is adjusted downward (lower value). These new dose limits are sometimes referred to as target doses.Their actual values depend on the values of the standard deviations determined above, and the economics of the process under consideration (Mehta 1992; IAEA 2002). These revised “dose limits” (or target doses) sometimes place severe restrictions on the process, which can be alleviated by reducing the process variability, for example by selecting a dosimetry system with a reduced uncertainty (that is, with higher precision and accuracy). Reference Monitoring Location For some radiation processes, the position of Dmin is inside the product carrier and not on the surface; hence, placement of dosimeters at these positions for process control during routine irradiation (see below) might be impossible without taking apart the carrier. For such cases, a convenient reference-monitoring location should be selected on the surface of the carrier, or outside but close to the carrier, for routine process control. The essential requirement during process qualification is that the relationships between the dose at this alternative reference location and the dose extremes be established, shown to be reproducible, and documented.

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Routine Process Control To assure that the process is being correctly administered, that is, all product is receiving dose within the specified range, certain process control procedures are in place at the irradiation facility.The following are principal elements in process control: • • • •

monitoring of all key process parameters routine product dosimetry product control product release and certification

Process Parameters All key process parameters that affect dose in the product are controlled and monitored (IAEA 2002). In a well-designed irradiation facility, these parameters are monitored from a control console and recorded automatically and continuously. Modern information technology has contributed significantly toward reliable control and recording of relevant parameters (Gibson and Levesque 2000; Comben and Stephens 2000). Routine Product Dosimetry One of the fundamental elements of process control is routine dosimetry.To allow the facility operator to certify the dose received by the product, routine dosimetry of each and every production run is essential (IAEA 2002).This provides a system that relevant authorities worldwide can rely on to ensure that imported food products have been treated according to the legal requirements. Dosimetry data may also be required in the event of mechanical failures and operational anomalies. For a gamma-ray facility operating in a continuous mode (for example, a shuffle-dwell system in which a single carrier cannot be removed independently from the irradiation chamber), it is recommended that there is always at least one product carrier inside the irradiator that contains one dosimeter or a dosimeter set. For a dosimeter set consisting of more than one dosimeter, the average value is taken as the dose at that location.Also, one dosimeter or a dosimeter set should be placed on the first and the last carrier of the production run.When operating in a batch mode, routine dosimeters should be placed on several carriers that are evenly distributed throughout the batch to generate statistically meaningful data. For incremental-dose systems, in which a single carrier can be removed independently from the irradiation chamber, it is recommended that one dosimeter or one dosimeter set be placed on each carrier.This is to minimize the loss of product in the event of a serious failure during the

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process. For an electron facility, there should always be one dosimeter set at the start of a production run. For long runs, one dosimeter or one dosimeter set should also be placed near the middle of the run and at the end of the run, and at other intervals as appropriate (Mehta and others 1993; Cabalfin and others 1991). In general, more frequent placement of dosimeters during a production run could result in less product rejection in the case of operational uncertainty or failure. Routine dosimeters should be placed either at the location of minimum dose or at the reference monitoring locations identified during process qualification. After the process, the dosimeters should be read and the corresponding dose values determined and compared against the values determined during process qualification. For process control, the accuracy of the measured absorbed dose is of essence. For reliable measurements, it is important to handle the dosimeters before, during, and after irradiation in controlled environment as specified in the facility’s operating procedures or in the manufacturer’s instructions. Product Control Plant design and administrative procedures should ensure that it is impossible to mix irradiated and nonirradiated product. In a well-designed irradiation facility, the areas for storing nonirradiated product are physically isolated from the areas where treated product is stored or handled. This also simplifies the product inventory control procedures. In some applications, radiation-sensitive (sometimes referred to as go/ no-go) indicators (which change color upon irradiation) may be used to show that a product has been exposed to a radiation source (ISO/ASTM 2004g). This practice does not, however, replace the routine product dosimetry discussed above because these are only qualitative indicators of irradiation. In addition, the color change is not always stable after irradiation and may in fact be affected by light or heat.Thus, indicators are useful only within the irradiation facility where these conditions are controlled. It must be emphasized that although these indicators can conveniently be used to assist in product inventory control, they must never be used to replace other inventory control procedures. Product Release and Certification Proper facility operation and adherence to process control procedures require records and documentation. Such records are necessary for the purpose of auditing by a customer or of inspection by an authority.These are reviewed by authorized individuals and maintained in the process documentation.Typically, these records should include (IAEA 2002):

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• information on calibration and maintenance of equipment and instrumentation used to control and measure dose delivered to the food product • all dosimetry data for process qualification, product absorbed-dose mapping, and routine product processing (including uncertainty in the dose values) • values of all process parameters affecting absorbed dose in the food product • product description and loading pattern in the carrier • date the product is processed, the name of the operator, and any special conditions of the irradiator that can affect dose to the product (such as process interruption) • copy of the shipping documents and of the certificate of irradiation Prior to the release of the irradiated food product for use, dosimetry data and recorded values of the key process parameters are examined to verify compliance with specifications. For each production run, the dose delivered to the product should be certified.

References ASTM. 2004b. Guide for Absorbed-Dose Mapping in Radiation Processing Facilities, E2302, Annual book of ASTM standards,Vol. 12.021,American Society for Testing and Materials International,West Conshohocken, PA, U.S.A. ASTM. 2004a. Standard Guide for Selection and Use of Mathematical Methods for Calculating Absorbed Dose in Radiation Processing Applications, E2232,Annual book of ASTM standards, Vol. 12.02, American Society for Testing and Materials International, West Conshohocken, PA, U.S.A. Biramontri, S.,Thongmitr,W.,Wanitsoksombut,W. 1989. Dosimetry for commissioning and quality control in the irradiation of onions.Appl. Radiat. Isot. 40:349–354 Cabalfin, E.G., Lanuza, L.G., Solomon, H.M. 1991. Process control and dosimetry in a multipurpose irradiation facility. Radiat. Phys. Chem. 55:781–784. Cavaco, M.C., Almeida, J.C., Andrade, M.E., Kovács, A., 1991. Dosimetry commissioning for an industrial cobalt-60 gamma radiation facility.Appl. Radiat. Isot. 42:1185–1188 Comben, M., Stephens, P. 2000. Irradiation plant control upgrades and parametric release. Radiat. Phys. Chem. 57:577–580. Gibson,W.H., Levesque, D. 2000. How gamma processing systems are benefiting from the latest advances in information technology. Radiat. Phys. Chem. 57: 581–585. IAEA. 2002. Dosimetry for food irradiation, TRS No. 409, International Atomic Energy Agency,Vienna. ICRU. 1984. Radiation dosimetry: Electron beams with energies between 1 and 50 MeV, ICRU Report 35, International Commission on Radiation Units and Measurements, Washington, D.C. ISO/ASTM. 2004d. Practice for Dosimetry in Gamma Irradiation Facilities for Food Processing, 51204, Annual book of ASTM standards, Vol. 12.02, American Society for Testing and Materials International,West Conshohocken, PA, U.S.A.

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ISO/ASTM. 2004b. Standard Guide for Selection and Calibration of Dosimetry Systems for Radiation Processing, 51261, Annual book of ASTM standards, Vol. 12.02, American Society for Testing and Materials International,West Conshohocken, PA, U.S.A. ISO/ASTM. 2004e. Practice for Dosimetry in Electron and Bremsstrahlung Irradiation Facilities for Food Processing, 51431, Annual book of ASTM standards, Vol. 12.02, American Society for Testing and Materials International, West Conshohocken, PA, U.S.A. ISO/ASTM. 2004g. Guide for Use of Radiation-Sensitive Indicators, 51539, Annual book of ASTM standards, Vol. 12.02, American Society for Testing and Materials International, West Conshohocken, PA, U.S.A. ISO/ASTM. 2004f. Practice for Dosimetry in an Electron-Beam Facility for Radiation Processing at Energies between 300 keV and 25 MeV, 51649,Annual book of ASTM standards, Vol. 12.02, American Society for Testing and Materials International, West Conshohocken, PA, U.S.A. ISO/ASTM. 2004c. Standard Guide for Estimating Uncertainties in Dosimetry for Radiation Processing, 51707, Annual book of ASTM standards, Vol. 12.02, American Society for Testing and Materials International,West Conshohocken, PA, U.S.A. ISO/ASTM. 2004a. Guide for Dosimetry in Radiation Research on Food and Agricultural Products, 51900, Annual book of ASTM standards, Vol. 12.02, American Society for Testing and Materials International,West Conshohocken, PA, U.S.A. Kovács,A., Moussa,A., Othman, I.,Alnaal, K. 1998. Dosimetry commissioning of the gamma irradiation facility ‘ROBO’. Radiat. Phys. Chem. 52:585–589 McLaughlin,W.L., Boyd,A.W., Chadwick, K.H., McDonald, J.C., Miller,A. 1989. Dosimetry for radiation processing. New York:Taylor and Francis. Mehta, K. 1992. Process qualification for electron-beam sterilization. Medical Device and Diagnostic Industry, June: 122–134. Mehta, K., Kovács,A., Miller,A. 1993. Dosimetry for quality assurance in electron-beam sterilization of medical devices. Medical Device Technology,April: 24–29. Mehta, K. 2002. Dosimetry uncertainty in radiation processing. Radiation Protection and Environment,Vol 25, No.2, 59–65. NPL. 1999. (National Physical Laboratory) Report CIRM 29, Guidelines for the Calibration of Dosimeters for Use in Radiation Processing,August 1999. Miller, A., Batsberg Pedersen, W. 1981. Dose distribution in electron irradiated plastic tubing. Radiat. Phys. Chem. 18:967–973. Polonia, I., Portugal, L.,Andrade, M.E. 1998. Dose mapping of dried figs treated by gammaradiation. Radiat. Phys. Chem. 52:569–573.

Notes 1. The Annual book of ASTM standards, Vol. 12.02 is published annually by ASTM International, although each standard is only updated about every five years.The reader is encouraged to seek the current version of the relevant ISO/ASTM or ASTM standard (www.astm.org).

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 8 MECHANISMS AND PREVENTION OF QUALITY CHANGES IN MEAT BY IRRADIATION Doug U. Ahn and E.J. Lee

Introduction Since the U.S.Army Medical Department began to assess irradiated food in 1955, many researchers have studied the safety of irradiated foods, and the World Health Organization (WHO) announced that irradiation of foods at <10 kGy is safe (WHO 1981). Currently, irradiation of food and agricultural products is allowed by about 40 countries, and approximately 60 commercial irradiation facilities are operating in the United States (Sommers 2004). In the United States, the Food and Drug Administration (FDA) has approved irradiation to eliminate insects and bacteria from wheat, flour, spices, and fruits; to control sprouting of potatoes and onions and ripening of fruits and vegetables; and to control trichinosis in pork. Irradiation was approved by the USDA to control Salmonella and other harmful bacteria in fresh and frozen poultry in 1992 (USDA 1992), and red meat products in 1999 (USDA 1999). Although irradiation is very effective in controlling foodborne pathogens, the adoption of irradiation technology by the meat industry is limited because of quality and health concerns about irradiated meat products. Irradiation produces a characteristic aroma as well as alters meat flavor and color that significantly impact consumer acceptance.The generation of a pink color in cooked poultry, brown/gray color in raw beef, and off-odor in meat and poultry by irradiation is a critical issue because consumers associate the presence of a pink color in cooked poultry breast meat and pork loin with contamination or being undercooked, the 127

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brown/gray color in raw beef with old or low-quality products, and offodor and off-flavor with undesirable chemical reactions. As a result, the meat industry has difficulties in using irradiation to achieve its food safety benefits. The government has made continuous research and consumer education efforts to establish that the use of irradiation is a safe process, and also has assured the public that irradiation does not result in any compositional changes in raw and cooked meat. However, when consumers find unusual color or odor/flavor changes in a familiar meat or meat product, this may cast unnecessary doubts in their minds as to what other changes may have occurred.Therefore, understanding the chemical changes in meat caused by irradiation and developing methods that can prevent those changes are important to improve consumer acceptance of irradiated meat.

Food Irradiation Food irradiation is a process in which radiation energy, which travels through space or matter in invisible waves, is applied to kill microorganisms or insects in foods (Josephson and Peterson 2000). Food irradiation under the recommended conditions does not involve the reaction of an atomic nucleus, but the electron cloud surrounding the nucleus initiates a chemical reaction. The primary effects are nonspecific and are produced by energetic electrons.They randomly hit any structure in the path of the incident or Compton electrons, without preference for particular atoms or molecules (Diehl 1995). Irradiation may result in one or more of three outcomes: ionization (removal of an electron), dissociation (loss of a hydrogen atom), or excitation (raising the energy of molecule to a higher energy level). For example, when energetic electrons pass through a sample of methane, they cause the primary effects.A strong interaction of the incident or Compton electrons with the methane molecule may cause ionization by removing an electron (e-), or dissociation by splitting off a hydrogen atom. A weak interaction may cause excitation of electrons, in which electrons have merely been promoted from low to higher internal energy levels. The major product of ionization reaction is free radicals that are usually very reactive. Because of the high reactivity of the free radicals produced as a result of the primary effect, the secondary effects will occur. The free radicals may undergo radical reactions such as recombination, electron capture, or dimerization. Disproportionation may also occur; what products will predominate depends on various conditions such as dose, dose rate, and temperature. The presence of oxygen or water and

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relative amounts of those can have a profound influence on the radiolytic process, producing a substance that may not have been present originally (Diehl 1995;Woods and Pikaev 1994). Although primary effects are largely nonspecific, secondary effects depend on specific chemical structures.A substance that readily reacts with free radicals is known as a scavenger, whereas a substance that produces a more reactive radical is a sensitizer. Energy is likely to be absorbed in the parts of the molecule with the greatest variation in electron density or where the bonds are weakest.Therefore, the products resulting from irradiation, heating, or other forms of energy input are often identical or similar (Diehl 1995). Two irradiation sources, cobalt-60 and electron beam, are commercially in use.

Microcidal Effect Radiation-induced cell death is mediated primarily through deposition of energy in a single event, a few vital macromolecules, or targets, the integrity of which is indispensable for proliferation. The genome DNA is generally regarded as the main target of ionizing and nonionizing radiation and extensive DNA damage following ionizing irradiation causes cell death (Alper 1977;Verma and Singh 2001). Another important mechanism of irradiation-induced cell death is associated with the ionizing radiation-generated reactive oxygen species, which result in oxidative damage to cell membrane (Mishra 2004). Radiolysis of water can produce a variety of reactive species (Thakur and Singh 1994). Hydrogen peroxide is an important reactive oxygen species that is one of the by-products of water radiolysis after exposure to ionizing radiation. The reaction of hydrogen peroxide with transition metals imposes on cells oxidative stress conditions that can result in damage to cell components such as proteins, lipids, and DNA, leading to mutagenesis and cell death (Asad and others 2004). The presence of oxygen almost always sensitizes cells to irradiation damage (Alper 1977). Irradiation also damages membrane structure, which interferes with the normal metabolism of cells, such as generation of energy, and inhibits cell growth and eventually leads to cell death (Alper 1977). The radiation-mediated lipid damage was modified by the inclusion of structure-modulating agents (for example, cholesterol) and antioxidants (for example, tocopherol, eugenol), and the magnitude of damage modification was determined by the concentration of these modifiers (Mishra 2004). The survival of microbial cells upon irradiation depends on the nature

130 Table 8.1.

Food Irradiation Research and Technology D-values of Foodborne Pathogens and Spoilage Bacteria

Pathogen

D10 (kGy)

Medium

A. hydrophila B. cereus (vegetative) C. jejuni E. coli O157:H7 L. monocytogenes

Y. enterocolitica Cl. botulinum (spore) C. sporogenes (spore)

0.17 0.14–0.19 0.18 0.25 0.42–0.55 0.57–0.65 0.51–0.59 0.38–0.50 0.42 0.39 0.11 3.56 6.3

Beef Beef Beef Beef Chicken Pork Beef Chicken Chicken Roast beef Beef Chicken Beef fat

M. phenylpyruvica P. putida S. faecalis

0.63–0.88 0.08–0.11 0.65–0.7

Chicken Chicken Chicken

Salmonella spp. Staph. aureus

Reference Palumbo and others 1986 Grant and others 1993 Clavero and others 1994 Clavero and others 1994 Huhtanen and others 1989 Grant and Patterson 1991 Monk and others 1994 Thayer and others 1990 Thayer and others 1992 Patterson 1988 El-Zawahry and others 1979 Anellis and others 1977 Shamsuzzaman and Lucht 1993 Patterson 1988 Patterson 1988 Patterson 1988

Adopted from the Journal of Food Protection 58(2). Monk, J.D., Beuchat, L. R., Doyle, M. P. Irradiation inactivation of food-borne microorganisms. p. 197–208. 1995,With permission from the Journal of Food Protection.

and extent of direct damage produced inside the cell, the number, nature, and longevity of irradiation-induced chemical species, and the inherent ability of cells to withstand the assaults and undergo repair.The DNA repair is a universal stress response following irradiation and operated via the RecA regulator of the SOS response (Fitt and Sharma 1991). Extracellular conditions such as pH, temperature, and chemical composition of the food in which microorganisms are suspended have very strong impact on the survival of microorganisms upon irradiation.The D10 values of foodborne pathogens and spoilage bacteria are shown in Table 8.1. Currently, irradiation can be used only in raw meat without any additives and the maximum irradiation doses for meats from different animal species and temperature conditions are different. Overall, ionizing radiation is an effective method to kill enteric pathogens associated with meat and poultry products.The populations of most common enteric pathogens such as C. jejuni, E. coli O157:H7, S. aureus, Salmonella spp., L. monocytogenes, and A. hydrophila can be significantly decreased or eliminated by low-dose (< 3.0 kGy) irradiation. Only enteric viruses and endospores of genera Clostridium and Bacillus are highly resistant to ionizing radiation, but even these are affected significantly by irradiation (Thayer 1995).

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Quality Changes in Meat by Irradiation A. Lipid Oxidation Irradiation is expected to accelerate lipid oxidation in meat because ionizing radiation generates hydroxyl radicals, a strong initiator of lipid oxidation, from meat (Thakur and Singh 1994). Irradiation-induced oxidative chemical changes are dose dependent, and the presence of oxygen has a significant effect on the development of oxidation and odor intensity (Merritt and others 1975). Irradiation accelerated lipid oxidation only when meat was irradiated and stored under aerobic conditions, especially in cooked meat. Hexanal, an off-flavor volatile typically associated with oxidative changes to linoleic acid, was detected only in aerobically packaged meat. This indicated that oxygen availability was more important for the development of lipid oxidation than irradiation (Ahn and others 1997, 2000a).Aldehydes contributed the most to oxidation flavor and rancidity in cooked meat, and hexanal was the predominant volatile aldehyde (Shahidi and Pegg 1994). The quality changes of frozen-stored irradiated meat were different from those of refrigerated storage (Nam and others 2002a). The irradiationdependent initiation of lipid oxidation was small in frozen turkey because the distribution of free radicals was minimal under frozen states.Taub and others (1979) reported that with less mobility in the frozen state, free radicals tend to recombine to form the original substances rather than diffuse through the food and react with other food components. Thus, the minimal lipid oxidation detected in frozen meat after irradiation should be due to the limited mobility of free radicals in frozen states (Nam and others 2002b). In conclusion, irradiation increased lipid oxidation of meat under aerobic conditions. However, oxygen played a more important role on the development of lipid oxidation in meat than irradiation, especially in cooked meat.

B. Sources and Mechanisms of Off-Odor Production Irradiation, Storage, and Packaging of Off-Odor Production in Meat All irradiated meat produced characteristic, readily detectable, irradiation odor regardless of degree of lipid oxidation (Ahn and others 1997, 1998b, 1999). Several off-odor volatile compounds were newly generated or increased in meat after irradiation (Patterson and Stevenson 1995;Ahn and others 2001). Hashim and others (1995) reported that irradiating uncooked chicken breast and thigh produced a characteristic “bloody and

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sweet” aroma that remained after the thighs were cooked but was not detectable after the breasts were cooked.Ahn and others (2000a) described the odor as “barbecued corn-like.” Champaign and Nawar (1969) found that hydrocarbons are the major radiolytic products in fat and are related to the fatty acid composition of the fat. Merritt and others (1978) postulated that carbonyls are formed in irradiated meats, due to the reactions of hydrocarbon radicals with molecular oxygen, which follows the same pathway as normal lipid oxidation. Batzer and Doty (1955) reported that methyl mercaptan and hydrogen sulfide were important to irradiation odor, and Patterson and Stevenson (1995) found that dimethyl trisulfide was the most potent off-odor compound, followed by cis-3- and trans-6-nonenals, oct1-en-3-one, and bis(methylthio-)methane in irradiated chicken meat. More recent studies showed that irradiation greatly increased or newly produced many volatile compounds such as 2-methyl butanal, 3-methyl butanal, 1-hexene, 1-heptene, 1-octene, 1-nonene, hydrogen sulfide, sulfur dioxide, mercaptomethane, dimethyl sulfide, methyl thioacetate, dimethyl disulfide, and trimethyl sulfide from meat (Jo and Ahn 1999, 2000b; Ahn and others 2000a; Fan and Ahn 2002; Nam and Ahn 2002b). The odor intensity of sulfur compounds was much stronger and more stringent than that of other compounds. Volatiles from lipids accounted for only a small part of the off-odor in irradiated meat (Lee and Ahn 2003). This indicated that sulfur-containing compounds would be the major volatile components responsible for the characteristic off-odor in irradiated meat, and supported the concept that the changes that occurred following irradiation were distinctly different from those of warmed-over flavor in oxidized meat. Ahn and others (2000a) reported that irradiated vacuum-packaged patties maintained irradiation off-odor during a two-week storage period, but the intensity of irradiation off-odor in aerobically packaged pork disappeared after one week or longer of refrigerated storage.This indicated that packaging played a very important role in the odor of irradiated meat. In conclusion, irradiation odor was different from lipid oxidation odor, and hydrocarbons and carbonyls played minor roles in irradiation offodor.The main source of irradiation off-odor was sulfur compounds derived from proteins, not lipids. Most of the sulfur-containing volatiles produced in meat by irradiation escaped during storage under aerobic packaging conditions. Irradiation and storage of meat in vacuum packaging may be desirable for long-term storage but may reduce the acceptance of irradiated meat because of the sustaining off-odor.

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Mechanism of Off-Odor Production in Irradiated Meat Ahn (2002) found that side chains of amino acids were susceptible to radiolytic degradation. Deamidation during irradiation is one of the main steps involved in amino acid radiolysis (Dogbevi and others 1999). The degradation of amino acids by oxidative deamination-decarboxylation via Strecker degradation produces branched-chain aldehydes (Mottram and others 2002), which may be the mechanism for the formation of 3-methyl butanal and 2-methyl butanal during irradiation from leucine and isoleucine, respectively (Jo and Ahn 2000a). Besides amino acids, fatty acids are also radiolyzed.When triglycerides or fatty acids are irradiated, hydrocarbons are formed by cutting CO2 and CH3COOH off from fatty acids in various free-radical reactions.The yield of these radiolytically generated hydrocarbons was linear with absorbed dose (Morehouse and others 1993). Radiolytic degradation of fatty acid methyl ethers was affected by irradiation dose, irradiation temperature, oxygen pressure, and fatty acid components (Miyahara and others 2002). Polyunsaturated fatty acids (PUFA) are more susceptible to radiolysis than monounsaturated or saturated fatty acids, and irradiation caused a significant reduction in PUFA (Formanek and others 2003). More than one site of amino acid side chains was susceptible to free radical attack, and many volatiles were produced by the secondary chemical reactions after the primary radiolytic degradation of side chains.The majority of newly generated and increased volatiles by irradiation were sulfur compounds, indicating that sulfur-containing amino acids are among the most susceptible amino acid groups to irradiation (Ahn and Lee 2002). The perception of odor from samples containing sulfur volatiles changed greatly depending upon their composition and amounts present in the sample.Sulfur compounds were produced not only by the radiolytic cleavage of side chains (primary reaction) but also by the secondary reactions of primary sulfur compounds with other compounds around them. The amounts and kinds of sulfur compounds produced from irradiated methionine and cysteine indicated that methionine is the major amino acid responsible for irradiation off-odor (Ahn 2002). Sensory panelists confirmed that all irradiated liposomes containing “sulfur amino acids” produced similar odor characteristics to irradiated meat, indicating that sulfur amino acids are mainly responsible for irradiation odor (Ahn 2002).The volatile profiles and sensory characteristics of amino acids clearly explained why irradiation odor was different from lipid oxidation odor, and why lipid oxidation was responsible for only a small part of the off-odor in irradiated meat (Ahn and others 1997, 1998a, 1999, 2000b). Jo and Ahn (1999) reported that the amount of volatiles released from oil emulsion correlated negatively with fat content.

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In conclusion, more than one site in amino acid side chains was susceptible to free radical attack, and many volatiles can apparently be produced by secondary chemical reactions after the primary radiolytic degradation of side chains. Only sulfur-containing volatiles, however, produced strong off-odor that was similar to irradiation odor of meat. The perception of odor from samples containing sulfur volatiles changed somewhat depending on the composition of other volatiles in the sample. Although some volatiles produced from nonsulfur amino acid homopolymers interacted with sulfur compounds, their roles in the odor characteristics of irradiated liposomes were minor. C. Color Changes in Meat by Irradiation Color Changes in Irradiated Raw and Cooked Meat The color changes in irradiated meat differ significantly depending on various factors such as irradiation dose, animal species, muscle type, and packaging type (Satterlee and others 1971; Shahidi and others 1991; Luchsinger and others 1996; Nanke and others 1999). Increased redness is a problem in irradiated light meats, especially cooked poultry breast and pork loin, whereas brown or gray discoloration is a problem in irradiated raw red meat under aerobic conditions. Irradiation increased redness (a* value) of both aerobically and vacuumpackaged raw chicken and turkey breast (Millar and others 1995; Nam and Ahn 2002a).The color changes were not localized in any specific area but evenly distributed over the whole meat sample. The increased redness was irradiation dose dependent and was stable during the two-week storage periods in raw turkey meat (Nam and Ahn 2002a). The increased red color in irradiated meat was more intense and stable with vacuum than aerobic packaging during refrigerated storage (Luchsinger and others 1996; Grant and Patterson 1991). Increased redness in raw meat by irradiation is not always detrimental, because the red color makes the irradiated meat look fresh (Lefebvre and others 1994). An objectionable red color in radiation-sterilized cooked chicken meat was found in the absence of oxygen (Hanson and others 1963). Irradiation increased the redness of vacuum packaged cooked turkey meat, but the surface color of aerobically packaged cooked meat was grayish brown regardless of irradiation. The pink color inside aerobically packaged cooked meat also changed to brown or yellow regardless of irradiation after two weeks of storage because of pigment oxidation (Nam and Ahn 2003b).Tappel (1957) noted that when precooked meat was irradi-

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Table 8.2. CIE Color a* Values of Irradiated Ground Beef Treated with Different Additives during Aerobic Storage at 4°C Nonirradiated

Irradiated

Control

Control

Ascorbic1

S+E2

A+S+E3

SEM

Pre-aged (0.17*) Day 1 Day 4 Day 7 SEM

22.0ax 20.1cy 20.1cy 0.4

17.4bx 17.0ex 14.8ey 0.3

21.3ay 24.5ax 25.6ax 0.4

17.4by 18.6dx 16.6dy 0.3

21.0a 22.3b 22.3b 0.4

0.3 0.4 0.4

Aged (0.31*) Day 1 Day 4 Day 7 SEM

19.7bx 19.4cx 15.4dy 0.3

17.3cx 16.9dx 15.3dy 0.3

22.7ay 25.9ax 26.1ax 0.4

19.4b 18.4c 18.2c 0.4

23.2a 23.3b 22.8b 0.4

0.3 0.4 0.4

Long-term-aged (0.81*) Day 1 19.8ax Day 4 8.1ey Day 7 8.4ey SEM 0.2

17.6bx 12.5dy 11.9dy 0.3

19.0ay 23.0ax 23.2ax 0.4

14.7cy 15.7cxy 16.2cx 0.4

17.2by 19.7bx 20.0bx 0.3

0.3 0.3 0.3

Storage

*Initial TBARS

value of meat (mg MDA/kg meat). acid 0.1%; 2Sesamol 100 ppm + ␣-tocopherol 100 ppm; 3Ascorbic acid 0.1% + Sesamol 100 ppm + ␣-tocopherol 100 ppm. a–eValues with different letters within a row are significantly different (P < 0.05). x–zValues with different letters within a column of the same sample are significantly different (P < 0.05). Adopted from the Journal of Food Science 68(5). 2003. Nam, K.C. and Ahn, D.U. Effects of ascorbic acid and antioxidants on the color of irradiated beef patties, p. 1686–1690. With permission from Institute of Food Technologists. 1Ascorbic

ated, the normal gray-brown hematin pigments were converted to uncharacteristic red pigments. In beef, color values were significantly influenced by the aging time. Color L* value increased as the aging time of beef increased. During storage after irradiation, L* values of ground beef also showed an increasing trend as the storage time increased, and the increase in L* value was more apparent in meat from “long-term-aged” beef than other ones (Nam and Ahn 2003c). Irradiation reduced the redness (a* value) of ground beef significantly, but to varying degrees depending on aging time (Table 8.2). Immediately after irradiation, the color of ground beef changed from a bright red to a greenish brown, which would be an unattractive beef color for consumers. Therefore, it is very difficult to implement irradiation technology in meat without controlling discoloration problems.

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Identification and Mechanism of Color Changes in Irradiated Meat Nanke and others (1998) proposed the color compound in irradiated meat as an oxymyoglobin (oxyMb)-like pigment. However, the red pigment cannot be an oxyMb because the red color formed by irradiation is produced in anoxic conditions. Nam and Ahn (2002a, 2000b) characterized the pink pigment formed in irradiated raw and cooked turkey breast as carbon monoxide-myoglobin (CO-Mb).They identified the pigment by comparing the absorption spectra of meat juice and myoglobin derivatives, and the reflectance spectra of meat surfaces.Three factors were essential for the pink color formation of light meats by irradiation: production of CO, generation of reducing conditions, and CO-Mb ligand formation.The formation of CO-Mb intensified the red color greatly. Nam and Ahn (2002a) reported that irradiation generated CO gas in both aerobically and vacuum-packaged meat, but the vacuum-packaged turkey breast showed higher CO than the aerobically packaged turkey breast. Most CO gas produced by irradiation escaped under aerobic conditions. Lee and Ahn (2004) reported that glycine, asparagine, glutamine, pyruvate, glyceraldehydes, ␣-ketoglutarate, and phospholipids were the major sources of CO production among meat components.The production of CO was via the radiolytic degradation of meat components and was closely related to the structure of component molecules. Nam and Ahn (2002a,2002b) showed that irradiation lowered oxidationreduction potential (ORP) of both aerobically and vacuum-packaged raw and cooked turkey breast meat. However, the ORP in irradiated meat increased rapidly during storage under aerobic conditions while maintained under vacuum-packaging conditions. Shahidi and others (1991) proposed that irradiation might increase the reducing potential of sodium ascorbate, and freshly irradiated pork patties had higher Hunter a* values than nonirradiated patties in vacuum packaging. Hydrated electrons (aqueous e-), a radiolytic radical, can act as a powerful reducing agent and react with ferricytochrome to produce ferrocytochrome (Swallow 1984). Giddings and Markakis (1972) proposed that oxymyoglobinlike pigment was formed by the reduction of heme iron by a radiolytic water product, hydrated electron, and the oxygenation from either residual oxygen or generated oxygen during irradiation.The decrease of ORP in meat played a very important role in CO-Mb formation because the CO-Mb complex can be formed only when heme pigment is in reduced form (Cornforth and others 1986). The mechanisms of color change in irradiated beef are different from those of light meats:The content of heme pigments in beef is about 10 times greater than that of light meats, and the proportion of carbon monoxide myoglobin (CO-Mb), the compound responsible for color

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changes in irradiated light meats, to total heme pigments in irradiated beef is small. Therefore, overall beef color is mainly determined by the status of heme pigments, which is determined by the reducing potential of meat. Irradiation of meat under vacuum conditions or addition of ascorbic acid to aerobically packaged meat creates reducing environments (Wheeler and others 1996) and can prevent brown color development in ground beef. In conclusion, irradiation increases the redness of light meat but turns the red meat color to brown under aerobic conditions. CO-heme pigment was the major color component responsible for the pink color in irradiated raw and cooked turkey breast, and the pigment formed was stable under vacuum packaging conditions. Irradiation generated CO and generated reducing conditions, which made it possible for the formation of CO-Mb complex and increased the intensity of pink color. In dark meat, however, the contribution of CO-heme pigment to the color of ground beef was much smaller than that of light meats. Therefore, the status of heme pigments determines the color of irradiated dark meat. Control of Off-Odor Production and Color Changes Additives Addition of antioxidants was very effective in inhibiting not only hydrocarbons but also volatile aldehydes in irradiated beef stored under aerobic conditions. Free radical terminators or metal chelating agents are commonly used in meat to reduce lipid oxidation and improve sensory quality of meat (Hsieh and Kinsella 1989; Chen and Ahn 1998). Huber and others (1953) found that the use of antioxidants such as ascorbate, citrate, tocopherol, gallic esters, and polyphenols was effective in reducing the off-odor of irradiated meat. Addition of acid to meat lowers the pH and increases the lightness of meat.The addition of citric or ascorbic acid did not affect the a values of irradiated meat but increased the L values, resulting in lighter overall color impression to meat (Xiong and others 1993; Nam and Ahn 2002b). Ascorbic acid incorporated to ground beef at the level of 0.1% (w/w) was very effective in maintaining redness (a* values) of irradiated ground beef, and the color-stabilizing effects of ascorbic acid were more distinct in “long-term-aged” than in “pre-aged” irradiated ground beef (Nam and Ahn 2003c). Satterlee and others (1971) reported that the formation of red, MbO2-like pigment formed from MbFe3+ was greatest in a nitrogen atmosphere, slightly inhibited in air and greatly inhibited in an oxygen atmosphere. Oxygen is an effective scavenger of aqueous electrons (eaq-).

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Therefore, in the absence of oxygen, a reducing environment is established in the irradiated meat, which converts ferric myoglobin to ferrous form (Giddings and Markakis 1972).The addition of ascorbic acid with or without sesamol + tocopherol significantly lowered the ORP values of irradiated ground beef regardless of the age of meat.The lowered ORP values by ascorbic acid maintained heme pigments in ferrous status and stabilized the color of irradiated ground beef. On the other hand, sesamol + tocopherol had no effect in preventing color changes and did not show any synergistic effect between ascorbic acid and sesamol + tocopherol in ground beef by irradiation (Nam and Ahn 2003c). Packaging Packaging turned out to be the major factor influencing the amounts and types of volatiles detected in irradiated meat (Ahn and others 2001). Nam and Ahn (2003a, 2003b) used a double-packaging concept to solve offodor problems in irradiated meat. In the double-packaging method, meat is individually packaged in an oxygen-permeable zipper bag and irradiated, or a few aerobically packaged meats are packaged again in a larger oxygen impermeable vacuum bag and irradiated.The meats irradiated in aerobic bags were vacuum-packaged one to three days after irradiation, and the outer vacuum bags of the double-packaged meats were removed a few days after refrigerated storage. Double-packaging was very effective in controlling both lipid oxidation–dependent (aldehydes) and radiolytic off-odor (S-compounds) volatiles.The a* value of double-packaged meats was lower than that of the vacuum-packaged meats, but was not enough to reduce the pink color of irradiated raw turkey meat. Packaging conditions were more critical in irradiated ground beef than light meat.The greenish-brown color was problematic when ground beef was irradiated under aerobic conditions, but anaerobic conditions protected the beef from discoloration. When vacuum-packaged irradiated beef was exposed to aerobic conditions in the middle of storage, the color bloomed to a vivid, fresh red and was maintained during the remaining aerobic storage (unpublished data). Packaging and Additive Combinations Addition of antioxidant to double-packaged irradiated meat was very effective in complementing the problem of double-packaging (Nam and Ahn 2003b): Sesamol+␣-tocopherol (S+E) and gallate+␣-tocopherol (G+E) combinations were very effective in preventing lipid oxidation in aerobically or double-packaged irradiated turkey during storage. Exposure of irradiated meat to aerobic conditions for three days eliminated most sulfur compounds. Double-packaging in combination with G+E or

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S+E significantly reduced the redness of irradiated cooked turkey breast meat, but G+E was more effective than S+E. The combined use of double-packaging (vacuum and then aerobic packaging) and ascorbic acid was very effective in not only reducing off-odor volatiles but also maintaining bright-red color of irradiated ground beef. Both irradiating under vacuum conditions and adding a reducing agent were helpful in maintaining low redox potential of irradiated beef and caused myoglobin to remain in a reduced form (unpublished data). In conclusion, antioxidants reduced lipid oxidation and volatile aldehydes significantly. Packaging was the most critical factor in the development of irradiation off-odor in meat.The combination of antioxidant and double-packaging was effective in controlling the oxidative quality changes of irradiated raw and cooked meat.

Future Research Although odor and color are important factors for consumer acceptance of irradiated raw meat, flavor and taste changes are important issues for cooked meat. Further processed or ready-to-eat (RTE) cooked meat products use various additives.Therefore, future research should elucidate the causes and mechanisms of flavor and taste changes, determine the roles of spices and additives in taste/flavor and microorganisms, and develop methods that can control taste/flavor changes in irradiated, further processed meat products.

References Ahn DU. 2002. Production of volatiles from amino acid homopolymers by irradiation. J Food Sci 67(7):2565–2570. Ahn DU, Olson DG, Jo C, Chen X,Wu C, Lee JI. 1998a. Effect of muscle type, packaging, and irradiation on lipid oxidation, volatile production and color in raw pork patties. Meat Sci 49:27–39. Ahn DU, Jo C, Olson DG. 2000a.Analysis of volatile components and the sensory characteristics of irradiated raw pork. Meat Sci 54:209–215. Ahn DU, Jo C, Olson DG, Nam KC. 2000b. Quality characteristics of pork patties irradiated and stored in different packaging and storage conditions. Meat Sci 56:203–209. Ahn DU, Lee EJ. 2002. Production of off-odor volatiles from liposome-containing amino acid homopolymers by irradiation. J Food Sci 67(7):2659–2665. Ahn DU, Nam KC, Du M, Jo C. 2001.Volatile production of irradiated normal, pale soft exudative (PSE) and dark firm dry (DFD) pork with different packaging and storage. Meat Sci 57:419–426.

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Ahn DU, Olson DG, Jo C, Love J, Jin SK. 1999.Volatiles production and lipid oxidation of irradiated cooked sausage with different packaging during storage. J Food Sci 64(2): 226–229. Ahn DU, Olson DG, Lee JI, Jo C,Wu C, Chen X. 1998b. Packaging and irradiation effects on lipid oxidation and volatiles in pork patties. J Food Sci 63(1):15–19. Ahn DU, Sell JL, Jeffery M, Jo C, Chen X,Wu C, Lee JI. 1997. Dietary vitamin E affects lipid oxidation and total volatiles of irradiated raw turkey meat. J Food Sci 62:954–959. Alper T. 1977.The role of membrane damage in radiation-induced cell death.Adv Exp Med Biol 84:139–165. Asad NR, Asad LMBO, de Almeida CEB, Felzenszwalb I, Cabral-Neto JB, Leitao AC. 2004. Several pathways of hydrogen peroxide action that damage the E-coli genome. Gen Mol Biol 27:291–303 Batzer OF, Doty DM. 1955. Nature of undesirable odors formed by gamma irradiation of beef. J Agric Food Chem 3:64–69. Champaign JR, Nawar WW. 1969.The volatile components of irradiated beef and pork fats. J. Food Sci. 34:335-339. Chen X,Ahn DU. 1998.Antioxidant activities of six phenolics from natural sources against lipid oxidation induced by Fe2+ or ultraviolet light (UV). J Amer Oil Chem Soc 75: 1717–1721. Cornforth DP, Vahabzadeh F, Carpenter CE, Bartholomew DT. 1986. Role of reduced hemochromes in pink color defect of cooked turkey rolls. J Food Sci 51:1132–1135. Diehl JF. 1995. In Safety of Irradiated Foods. 2nd Ed. Marcel Dekker, Inc., New York, NY. Dogbevi MK,Vachon C, Lacroix M. 1999. Physicochemical and microbiological changes in irradiated fresh pork loins. Meat Sci 51:349–354. Fan X, Sommers CH,Thayer DW, Lehotay SJ. 2002. Volatile sulfur compounds in irradiated precooked turkey breast analyzed with pulsed flame photometric detection. J Agric Food Chem 50:4257–4261. Fitt PS, Sharma N. 1991. Starvation as an inducer of error-free DNA repair in Escherichia coli. Mut Res 262:145–150. Formanek Z, Lynch A, Galvin K, Farkas J, Kerry JP. 2003. Combined effects of irradiation and the use of natural antioxidants on the shelf-life stability of overwrapped minced beef. Meat Sci 63:433–440. Giddings GG, Markakis P. 1972. Characterization of the red pigments produced from ferrimyoglobin by ionizing radiation. J Food Sci 37:361–364. Grant IR, Patterson MF. 1991. Effect of irradiation and modified atmosphere packaging on the microbiolical safety of minced pork stored under temperature abuse conditions. Int J Food Sci Technol 26:507–519. Hanson HL, Brushway MJ, Pool MP, Lineweaver H. 1963. Factors causing color and texture differences in radiation-sterilized chicken. Food Technol 17:1188–1194. Hashim IB, Resurreccion AVA, MaWatters KH. 1995. Disruptive sensory analysis of irradiated frozen or refrigerated chicken. J Food Sci 60:664–666. Hsieh RJ, Kinsella JE. 1989. Oxidation of polyunsaturated fatty acids: mechanisms, products, and inhibition with emphasis on fish.Adv Food Nutr Res 33:233–237. Huber W, Brasch A,Waly A. 1953. Effect of processing conditions on organoleptic changes in foodstuffs sterilized with high intensity electrons. Food Technol 7:109–115. Jo C, Ahn DU. 1999. Fat reduces volatiles production in oil emulsion system analyzed by purge-and-trap dynamic headspace/gas chromatography. J Food Sci 64(4):641–643. Jo C,Ahn DU. 2000a. Production of volatiles from irradiated oil emulsion systems prepared with amino acids and lipids. J Food Sci 65(4):612–616.

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Jo C,Ahn DU. 2000b.Volatiles and oxidative changes in irradiated pork sausage with different fatty acid composition and tocopherol content. J Food Sci 65:270–275. Josephson ES, Peterson MS. 2000. Preservation of food by ionizing radiation (II). Boca Raton, FL: CRC Press. p 102–103 Lefebvre N, Thibault C, Charbonneau R, Piette JPG. 1994. Improvement of shelf-life and wholesomeness of ground beef by irradiation 2: chemical analysis and sensory evaluation. Meat Sci 36:371–380. Lee EJ,Ahn DU. 2004. Sources and mechanisms of carbon monoxide production by irradiation. J Food Sci 69(6):c485–490. Lee EJ, Ahn DU. 2003. Production of off-odor volatiles from fatty acids and oils by irradiation. J Food Sci 68:(1):70–75. Luchsinger SE, Kropf DH, Garcia-Zepeda CM, Hunt MC, Marsden JL, Rubio-Canas EJ, Kastner CL, Kuecker WG, Mata T. 1996. Color and oxidative rancidity of gamma and electron beam irradiated boneless pork chops. J Food Sci 61(5):1000–1005, 1093. Merritt C Jr,Angelini P,Wierbicki E, Shuts GW. 1975. Chemical changes associated with flavor in irradiated meat. J Agric Food Chem 23:1037–1043. Merritt C Jr,Angelini P, Graham RA. 1978. Effect of radiation parameters on the formation of radiolysis products in meat and meat substances. J Agric Food Chem 26:29–36. Millar SJ, Moss BW, MacDougall DB, Stevenson MH. 1995.The effect of ionizing radiation on the CIELAB color co-ordinates of chicken breast meat as measured by different instruments. Int J Food Sci Technol 30:663–674. Mishra KP. 2004. Cell membrane oxidative damage induced by gamma-radiation and apoptotic sensitivity. J Environ Pathol Toxicol Oncol 23:61–66. Miyahara M, Saito A, Kamimura T, Nagasawa T, Ito H,Toyoda M. 2002. Hydrocarbon productions in hexane solutions of fatty acid methyl esters irradiated with gamma rays. J Health Sci 48:418–426. Monk JD, Beuchat LR, Doyle MP. 1995. Irradiation inactivation of food-borne microorganisms. J Food Protec 58(2):197–208. Morehouse KM, Kiesel M, Ku Y.1993. Identification of meat treated with ionizing radiation by capillary gas-chromatographic determination of radiolytically produced hydrocarbons. J Agric Food Chem 41:758–763. Mottram DS,Wedzicha BL, Dodson AT. 2002.Acrylamide is formed in the Maillard reaction. Nature 419:448–449. Nam KC,Ahn DU. 2002a. Carbon monoxide-heme pigment complexes are responsible for the pink color in irradiated raw turkey breast meat. Meat Sci 60(1):25–33. Nam KC, Ahn DU. 2002b. Mechanisms of pink color formation in irradiated precooked turkey breast. J Food Sci 67(2):600–607. Nam KC,Ahn DU. 2002c. Effect of double-packaging and acid combination on the quality of irradiated raw turkey patties. J Food Sci 67(9):3252–3257. Nam KC,Ahn DU. 2003a. Combination of aerobic and vacuum packaging to control color, lipid oxidation and off-odor volatiles of irradiated raw turkey breast. Meat Sci 63(3): 389–395. Nam KC, Ahn DU. 2003b. Use of double-packaging and antioxidant combinations to improve color, lipid oxidation, and volatiles of irradiated raw and cooked turkey breast patties. Poult Sci 82(5):850–857. Nam KC, Ahn DU. 2003c. Effects of ascorbic acid and antioxidants on the color of irradiated beef patties. J Food Sci 68(5):1686–1690. Nam KC, Min BR, Park KS, Lee SC,Ahn DU. 2003. Effects of ascorbic acid and antioxidants on the lipid oxidation and volatiles of irradiated beef patties. J Food Sci 68(5):1680–1685.

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Nam KC, Kim YH, Du M, Ahn DU. 2002b. Off-odor and pink color development in precooked, ionizing-radiated turkey breast during frozen storage. Poult Sci 81(2):269–275. Nam KC, Hur SJ, Ismail H,Ahn DU. 2002a. Lipid oxidation, volatiles, and color changes in irradiated turkey breast during frozen storage. J Food Sci 67(6):2061–2066. Nanke KE, Sebranek JG, Olson DG. 1998. Color characteristics of irradiated vacuumpackaged pork, beef, and turkey. J Food Sci 63(6):1001–1006. Nanke KE, Sebranek JG, Olson DG. 1999. Color characteristics of irradiated aerobically packaged pork, beef, and turkey. J Food Sci 64:272–276. Patterson RL, Stevenson MH. 1995. Irradiation-induced off-odor in chicken and its possible control. Br Poult Sci 36:425–441. Satterlee LD,Wilhelm MS, Barnhart HM. 1971. Low dose gamma irradiation of bovine metmyoglobin. J Food Sci 36(3):549–551. Shahidi F, Pegg RB, Shamsuzzaman K. 1991. Color and oxidative stability of nitrite-free cured meat after gamma irradiation. J Food Sci 56:1450–1452. Shahidi F, Pegg RB. 1994. In: Lipids in food flavors. ACS Sym Ser 558. Am Chem Soc, Washington, D.C., p. 256–279. Sommers CH. 2004. Food irradiation is already here. Food Technol 58(11):22. Swallow AJ. 1984. In: Recent Advances in the Chemistry of Meat. The Royal Soc Chem: Burlington, London, UK. p. 165–175. Tappel AL. 1957.The red pigment of precooked irradiated meats. Food Res 22:408–412. Taub IA, Kaprielian RA, Halliday JW,Walker JE,Angelini P, Merritt Jr C. 1979. Factors affecting radiolytic effects in food. Radio Phys Chem 14:639–953. Thakur BR, Singh RK. 1994. Food irradiation—Chemistry and applications. Food Rev Int 10(4):437–473. Thayer DW. 1995. Use of irradiation to kill enteric pathogens on meat and poultry. J Food Safety 15:181–192. USDA FSIS. 1992. Irradiation of poultry products. Federal Register 57:43588–43600. USDA. 1999. Meat and poultry irradiation proposal. USDA-FSIS www.fsis.usda.gov/oa/background/irradprop.htm Verma NC, Singh RK. 2001. Stress-inducible DNA repair in Saccharomyces cerevisiae. J Env Pathol Toxicol Oncol 20:1–7. Wheeler TL, Koohmaraie M, Shackelford SD. 1996. Effect of vitamin C concentration and co-injection with calcium chloride on beef retail display color. J Anim Sci 74(8):1846–1853. WHO. 1981.Wholesomeness of Irradiated Foods.Technical Report Series 659. Geneva. Woods RJ, Pikaev AK. 1994. Selected topics in radiation chemistry. In: Applied radiation chemistry: radiation processing.Woods RJ, Pikaev AK, eds. New York: John Wiley & Sons, Inc. p. 165–210. Xiong YL, Decker EA, Robe GH, Moody WG. 1993. Gelation of crude myofibrillar protein isolated from beef heart under antioxidant conditions. J Food Sci 58:1241–1244.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 9 IRRADIATION AS A PHYTOSANITARY TREATMENT FOR FRESH HORTICULTURAL COMMODITIES: RESEARCH AND REGULATIONS Peter A. Follett and Robert L. Griffin

Introduction A quarantine pest is a plant pest of potential economic importance to an area in which the pest is not yet present, or is present but not widely distributed and is being officially controlled. Quarantine or phytosanitary treatments eliminate, sterilize, or kill regulatory pests in exported commodities to prevent their introduction and establishment into new areas. Irradiation is a versatile technology to disinfest fresh and durable agricultural commodities of quarantine pests. Irradiation is broadly effective against insects and mites, cost competitive with other disinfestation methods, (such as fumigation, heat and cold) and fast. Irradiation generally does not significantly reduce commodity quality at the doses used to control insect pests, and may even extend shelf-life. Additionally, irradiation can be applied to the commodity after packaging. Unlike other disinfestation techniques, irradiation does not need to kill the pest immediately to provide quarantine security, and therefore live (but sterile) insects may occur with the exported commodity, making inspection for the target pests redundant as a confirmation of treatment application and efficacy. This places an added level of importance on the certification procedures for irradiation facilities and proper documentation accompanying each shipment confirming treatment at approved

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doses. It also places an onus on researchers to ensure that the minimum absorbed dose approved for each quarantine pest has an adequate margin of safety. The history of quarantine uses of irradiation and the relative tolerance of various arthropod groups have been reviewed by Rigney (1989), Heather (1992), Burditt (1996), and Hallman (1998, 2001). In this review we provide an update and synthesis of previous information, and discuss current trends in the use of irradiation as a phytosanitary treatment, with an emphasis on research methodology and the regulatory framework.

Developing Irradiation Quarantine Treatments Insect Radiotolerance Ionizing energy breaks chemical bonds within DNA and other molecules, thereby disrupting normal cellular function in the insect. Insect response to irradiation varies with the insect species and life stage, and the absorbed dose received by the insect.Tissues with undifferentiated, actively dividing cells are most susceptible to irradiation. Consequently, eggs are normally the most susceptible life stage and adults are the most tolerant. Insect gonads and midgut contain mitotically active tissues, and irradiated insects are often sterile and stop feeding soon after treatment (Ducoff 1972; Tilton and Brower 1983; Koval 1994; Nation and Burditt 1994). Arthropod groups vary in their tolerance to irradiation (Table 9.1). Among insects, Diptera (flies), Coleoptera (beetles), and Hemiptera (true bugs) tend to be less radiotolerant than Lepidoptera (moths and butterflies), although there is considerable variation among the species that have been tested within these groups. Estimates for Hemiptera (scales, mealybugs, aphids, and whiteflies) and Thysanoptera (thrips) are based on a small number of studies. Two of the most radiotolerant insects are the Indianmeal moth, Plodia interpunctella, and the Angoumois grain moth, Sitrotroga cerealella, both stored products pests (Ahmed 2001; Ignatowicz 2004). Several species of mites have been tested and appear to be relatively tolerant of ionizing radiation. Nematodes are highly tolerant. Few studies have conducted the large-scale tests needed to confirm the efficacy of an irradiation dose predicted to give 100% mortality.Table 9.2 provides a list of quarantine insect pests that have been rigorously tested; much of this information is recent and will be used to update and revise approved irradiation treatment doses for specific pests. Most insects are sterilized at doses below 300 Gy.

Irradiation as a Phytosanitary Treatment Table 9.1.

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Range of Doses Predicted to Control Various Pest Groups

Pest Group

Required Response

Hemiptera

Sterilize adult or prevent generation turnover Sterilize actively reproducing adult Prevent adult emergence from larva Sterilize actively reproducing adult Sterilize actively reproducing adult Sterilize actively reproducing adult Sterilize actively reproducing adult Sterilize actively reproducing adult Prevent adult emergence from larva Sterilize adult from late pupa Sterilize actively reproducing adult Sterilize actively reproducing adult

Thrips Tephritid fruit flies Bruchid seed weevils Curculionid weevils Scarab beetles Stored product beetles Stored product moths Lepidopteran borers Mites Nematodes

Dose Range (Gy) 50–250 150–350 50–150 70–300 80–150 50–150 50–250 100–600 100–250 200–400 200–400 ~ 4,000

Modified from International Plant Protection Convention (2003a) “Guidelines for the use of irradiation as a phytosanitary measure.”

Methodology The goal of irradiation as a phytosanitary treatment is to provide quarantine security for any regulated pests residing in or on the exported commodity. This is most often accomplished by preventing development to the reproductive stage or sterilizing the reproductive stage of the insect. If multiple species on a commodity are regulated pests, irradiation studies begin by comparing the tolerance of the quarantine pests; then, in-depth studies focus on the most tolerant stage of the most tolerant species to arrive at a single dose providing quarantine security for the commodity. Typically, the most advanced developmental stage of the insect occurring in the commodity is the most tolerant when the goal is preventing adult emergence or reproduction. The most advanced stage may be the larva (or nymph), pupa, or adult.When larval development is completed in the host but the insect pupates outside the host, irradiation is applied to prevent adult emergence. In the case of tephritid fruit flies, preventing adult emergence is the desired response required for regulatory purposes because it prevents the emergence of adult flies that could be trapped and trigger regulatory actions, despite being sterile.When the insect pupates in the host, preventing adult emergence may be difficult, so adult sterility is the goal. Often adults occur with the commodity. When the adult stage can

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West Indies fruit fly sapote fruit fly guava fruit fly

A. obliqua A. serpentina A. striata A. suspensa Bactrocera dorsalis

melon fly

Jarvis’ fruit fly solanaceous fruit fly Queensland fruit fly

Mediterranean fruit fly

apple maggot plum curculio

B. cucurbitae

B. jarvisi B. latifrons B. tryoni

Ceratitis capitata

Rhagoletis pomonella Conotrachelus nenuphar

oriental fruit fly

Mexican fruit fly

Common Name 100 69 100 100 100 50 250 150 125 210 150 101 150 75 101 250 218 150 100 57 92

Target Dose L L L L L L L L L L L L L L L L L L L L A

Stage 101,794 95,000 100,400 105,252 13,094 100,000 620,000 173,000 55,743 169,903 93,666 153,814 157,111 24,700 138,635 110,800 70,400 100,854 31,920 22,360 25,000

# Tested

Bustos et al. 2004 Hallman & Martinez 2001 Bustos et al. 2004 Bustos et al. 2004 Toledo et. al. 2003 Gould & von Windeguth 1991 Seo et al. 1973 Komson et al. 1992 Follett & Armstrong 2004 Seo et al. 1973 Follett & Armstrong 2004 Heather et al. 1991 T. Phillips (unpublished) Rigney and Wills 1985 Heather et al. 1991 Seo et al. 1973 Seo et al. 1973 Bustos et al. 2004 Follett & Armstrong 2004 Hallman 2004 Hallman 2003

Reference

Insects for Which Large-Scale Confirmatory Testing Has Been Performed to Establish Treatment Efficacy

Anastrepha ludens

Species

Table 9.2.

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West Indian sweetpotato weevil sweetpotato vine borer codling moth oriental fruit moth false spider mite koa seedworm

Euscepes postfasciatus Omphisa anastomosalis Cydia pomonella Grapholita molesta Brevipalpus chilensis Cryptophlebia illepida

Stage: L, larva; P, pupa;A, adult.

sweetpotato weevil

Common Name 150 165 150 150 200 232 300 250

Target Dose A A A P L L A L

Stage 62,600 30,655 50,000 12,000 132,000 58,779 8,042 11,256

# Tested

Follett (in press) Hallman 2001 Follett (in press) Follett (in press) Mansour & Mohamad 2004 Hallman 2004 Castro et al. 2004 Follett and Lower 2000

Reference

Insects for Which Large-Scale Confirmatory Testing Has Been Performed to Establish Treatment Efficacy (continued)

Cylas formicarius elegantulus

Species

Table 9.2.

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occur in the commodity and is the most tolerant stage, the measure of treatment efficacy is the level of sterility. For sexually reproducing species, sterilizing one sex may be sufficient to prevent reproduction, but both sexes must be sterilized if mating status is unknown, as is usually the case. Males are often but not always more tolerant than females. Reciprocal crosses between irradiated and control males and females at several sub-sterilizing doses are useful to determine the more tolerant sex (Follett and Lower 2000). In large-scale confirmatory tests, males and females should be mated before treatment, and females should have begun ovipositing. After irradiation treatment, surviving males and females are combined and allowed to mate and reproduce to determine the success of the dose. Adult females irradiated at a sterilizing dose will often oviposit (particularly if they were gravid when irradiated), but eggs will not hatch or hatching neonates do not develop.With asexual species the female is the focus of all tests. In rare cases irradiated insects will recover, so it is important to continue tests until all insects have died. Many insect species have life history attributes that complicate testing methods. For example, diaspidid scale insects are sessile (attached to the plant) and long-lived, and so experiments must use host material (for example, pumpkin) that does not deteriorate after irradiation treatment and before the insects die. Some species require live host material to survive. The long-lived semi-sessile coccid scale, green scale (Coccus viridis), survives only on live host material such as gardenia, coffee, and hibiscus, which complicates testing because irradiation treatment causes rapid plant deterioration (Hara et al. 2002). Diapausing and nondiapausing strains of insects may have different tolerances to radiation and may require different bioassay methods (Hallman 2003). To determine the most tolerant stage for a species, all stages are treated with a range of irradiation doses. Generally, five doses should be selected and five replicates of at least 30–50 insects should be used. In some cases a single diagnostic dose is used to separate tolerance among stages or species.The ideal diagnostic dose causes only moderate mortality in the stage or species predicted to be most tolerant.This improves the chances that statistical tests can be used to separate mean responses among groups.Tests should be designed with the biology of the insect in mind, and insects should always be tested in the commodity of interest if possible. For example, pupae may be inherently more tolerant of irradiation than larvae, but because they occur only at the surface of the fruit, they may be easier to sterilize than larvae that feed at the center of the fruit where hypoxic conditions exist. If artificial inoculation is used, insects should be placed where they occur naturally or be allowed time to redistribute to preferred feeding sites in the commodity.

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Accurate dosimetry is critical to the success of insect irradiation studies. The objective in research is to minimize the dose uniformity ratio (DUR), typically to keep it less than 1.2:1. Mehta and O’Hara discuss dosimetry in detail elsewhere in this text. Dosimeters should be placed where the insects occur to accurately measure absorbed doses. After dose response tests are completed, large-scale tests are conducted with the most tolerant life stage at a dose predicted to cause 100% mortality. The dose determined to provide quarantine security from testing large numbers of insects is often higher than that predicted from small-scale dose response tests to give 100% mortality. Insects are irradiated in the commodity after inoculation with a known number of insects or in naturally infested host material. For internal feeding insects naturally infesting the commodity, the number of viable insects treated is estimated by the number of insects successfully emerging in paired samples of untreated controls. Untreated control insects are always included in tests with irradiated insects so that mortality can be adjusted for natural variation and to guard against changes in experimental conditions over the course of testing that cause higher than normal mortality. Although control mortality ⱕ 20% is desirable, higher mortality may be normal when using wild insects and naturally infested commodities. Probit analysis is the standard method to evaluate dose response data, but other models (for example, logit) should be used if they provide a better fit to the data (Robertson and Preisler 1992). These analyses are used to compare radiotolerance among life stages or species, and to help identify a target dose for large-scale testing. Covariance analysis is an alternative to compare response among stages or between species. Covariance analysis requires the slopes of the regression lines fitted to each group to be parallel, so the test of parallelism (nonsignificant stage or species by dose interaction effect) is tested before comparing stage or species effects (for example, Follett 2004). As mentioned, the actual dose to achieve quarantine security at a given level of precision may exceed the dose predicted from small-scale dose response tests. For example, the dose predicted to prevent emergence of adult melon flies treated in papaya from dose response data was 90 Gy (0 survivors in 900 tested insects) (Follett and Armstrong 2004); however, subsequent large-scale testing at 120 Gy resulted in 1 survivor out of 50,000 treated third instars and several partially emerged pupae. Increasing the dose for large-scale testing to 150 Gy resulted in 0 survivors in 96,700 treated insects and no partial pupal emergence (Follett and Armstrong 2004).These results demonstrate the need for large-scale testing to verify a dose.

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Varietal Testing When the pest infests more than one host cultivar or variety, disinfestation studies should theoretically be carried out on the variety in which the pest is most tolerant to irradiation. For a given absorbed dose, pest response to irradiation in the host may vary depending on the milieu surrounding the pest.As mentioned, oxygen concentration is known to modify sensitivity to irradiation, and conditions producing hypoxia can increase radiation tolerance (Alpen 1998). Fruit flies have higher radiotolerance when treated in a nitrogen atmosphere compared with ambient air (Fisher 1997) and when treated in fruit compared with diet (Follett and Armstrong 2004). Radiation damage and mortality was less in codling moth larvae treated in 0.25% O2 compared with 3% O2 (Batchelor 1989). Varieties of a commodity with higher water content may have lower available oxygen, and insects infesting these varieties might show higher radiotolerance.Variety was shown to have a dramatic effect on egg hatch and larval development during irradiation studies with the Mediterranean fruit fly in nectarines (eight varieties) and plums (four varieties) (Kaneshiro et al 1985), and a link with fruit moisture content was suspected but not measured. In the absence of comparative tests among varieties, the variety at greatest risk of infestation or the variety that makes up the greatest proportion of trade is used.

Probit 9 Efficacy and Alternatives Postharvest commodity treatments for pests requiring a high degree of quarantine security are commonly referred to as probit 9 treatments.A response at the probit 9 level results in 99.9968% response.The USDA has used 99.9968% efficacy as the basis for approving many quarantine treatments against tephritid fruit flies. Probit 9, or 99.9968%, mortality is often incorrectly interpreted to mean that three survivors are allowed in 100,000 treated insects or 32 survivors in 1 million treated insects (Baker 1939) without regard to the precision associated with this level of survivorship.To achieve probit 9 mortality at the 95% confidence level,93,613 insects must be tested with no survivors. Quantitative methods have been developed to calculate the number of test insects and confidence limits for other levels of precision and treatment efficacy, with and without survivors (Couey and Chew 1986).A probit 9 treatment usually provides adequate quarantine security (but see Mangan et al. 1997; Powell 2003), and developing such a treatment frequently proves to be the quickest and most easily accepted method for overcoming phytosanitary restrictions.

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Other countries (Japan,Australia,New Zealand) accept quarantine treatment efficacy at 99.99% (at the 95% confidence level), which is obtained by treating 29,956 insects with no survivors (Couey and Chew 1986). Japan and New Zealand require three replicates of 10,000 test insects with no survivors (Sproul 1976).The number of insects tested may need to be adjusted (increased) to account for control mortality (Follett and Neven, 2006). For insects that are difficult to obtain in the field or rear in the laboratory, testing the efficacy of a potential treatment using lower numbers may be acceptable in certain cases. For example, an irradiation treatment of 300 Gy was accepted for the mango seed weevil,Sternochetus mangiferae (Federal Register 2002), a monophagous pest of mangos, based on evidence for its limited potential impact in the United States (Follett and Gabbard 2000) and cumulative data from several studies with a few thousand insects showing prevention of adult emergence at a target dose of 300 Gy (Heather and Corcoran 1992; Follett and McQuate 2001) and sterilization at lower doses (Seo et al. 1974; Follett and McQuate 2001).When low numbers of insects are used, the number tested without survivors can be used to calculate the level of quarantine security. When dose response or small-scale tests are used to predict an irradiation dose to control the pest, the lowest effective dose should be increased by 20–25% to add a margin of safety. Landolt et al. (1984) pointed out that the probit 9 standard may be too stringent for commodities that are rarely infested or poor hosts. The alternative treatment efficacy approach measures risk as the probability of a mating pair or reproductive individual surviving in a shipment.The main quantitative argument for deviating from probit 9 treatment efficacy is low infestation rate of the commodity, but many other biological and nonbiological factors affect risk (Vail et al. 1993; Whyte et al. 1994; Follett and McQuate 2001). An advantage to using the alternative treatment efficacy approach is that fewer insects may be needed during development of quarantine treatments (Follett and McQuate 2001).The alternative treatment efficacy approach fits with the systems approach where multiple procedures are used to cumulatively provide quarantine security (Jang and Moffitt 1994). For example, irradiation of avocados within the range of doses providing probit 9 kill of tephritid fruit flies and other pests (100–400 Gy) causes discoloration to the fruit flesh. In Hawaii, the oriental fruit fly is the main quarantine pest of avocados, although the avocado fruit on the tree is a poor host for fruit flies.Whereas 120 Gy is required to give probit 9 efficacy (prevent adult emergence) for the oriental fruit fly, irradiation treatment at a dose of 80 Gy provides >99% efficacy (Follett and Armstrong 2004) and potentially could be combined with poor host status, inspection, field control, and other mitigation procedures to give a high level of quarantine security.

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Maximum pest limit is another approach to quarantine security that focuses on survival rather than mortality and is closely related to the alternative treatment efficacy approach (Baker et al. 1990; Mangan et al. 1997). It is defined as the maximum number of insects that can be present in a consignment imported during a specified time at a specified location (Baker et al. 1990).A minimum sample size for inspection is determined from an estimate of the level of pest infestation, the efficacy of the postharvest treatment, and the maximum lot size assembled per day at a location.This level of inspection is predicted to detect infestation levels greater than the maximum level of permissible infestation with a certain probability and confidence limits (Baker et al. 1990).

Generic Treatments A “generic” quarantine treatment is one that provides quarantine security for a broad group of pests. From a regulatory standpoint, “generic” can also refer to a treatment for a pest on all commodities it infests.A generic treatment for a group of insects could be applied at many taxonomic levels, for example, to all Diptera (flies), or to flies in the family Tephritidae (fruit flies), or to tephritid fruit flies in the genus Bactrocera. Irradiation is the ideal technology for developing generic treatments because it is effective against most insects and mites at dose levels that do not affect the quality of most commodities. Before a generic treatment can be recommended, information is needed on effective irradiation doses for a wide range of insects within the taxon. Initially, development of the generic dose concept has focused on tephritid fruit flies.The International Consultative Group on Food Irradiation (ICGFI) was the first group to formalize a recommendation for generic irradiation treatments (ICGFI 1991). In 1986, based on irradiation data for several tephritid fruit fly species and a limited number of other insect pests, they proposed a dose of 150 Gy for fruit flies and 300 Gy for other insects.Adoption of the 150 Gy dose for fruit flies was stymied by research suggesting that three tephritid fruit fly species in Hawaii required higher irradiation doses to prevent adult emergence from infested fruit (Seo et al. 1973). Based on the data presented by Seo et al. (1973), USDA-Animal Plant Health Inspection Service (APHIS) approved irradiation doses of 210, 225, and 250 Gy for the melon fly, Mediterranean fruit fly, and oriental fruit fly, respectively, for exporting fruits and vegetables from Hawaii (Federal Register 1997).The majority of economically important tephritid fruit flies come from four genera—Anastrepha, Bactrocera, Ceratitis, and Rhagoletis, and irradiation studies have been con-

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ducted with species in each of these genera. Although results from various irradiation studies with fruit flies have not always been consistent (reviewed by Burditt 1994, 1996; Rigney 1989; Hallman and Loaharanu 2002), the preponderance of evidence suggested that all the species in these genera could be controlled by doses at or below 150 Gy. Recently, Follett and Armstrong (2004) demonstrated that irradiation doses of 100, 125, and 150 Gy controlled C. capitata, B. dorsalis, and B. cucurbitae, respectively, which supported lowering the dose for Hawaii’s fruit flies and acceptance of the proposed 150 Gy generic dose for tephritids. A proposed rule from USDA-APHIS is in preparation, recommending a generic dose of 150 Gy for all tephritid fruit flies. This will be the first widespread use of a generic phytosanitary treatment for any pest group or treatment type. The generic dose concept has been applied on a limited scale to irradiation treatment for fruits exported from Hawaii to the U.S. mainland. In 2001, the USDA-APHIS convened a meeting to establish treatment protocols for a new commercial irradiation facility (Hawaii Pride LLC) in Hawaii, and approved generic irradiation doses of 250 Gy for any species of Tephritidae (fruit flies) and Thysanoptera (thrips); and 400 Gy for any species of Coccidae (soft scales), Pseudococcidae (mealybugs), and immature Lepidoptera (moths) infesting eight fruits being exported to the U.S mainland. In this case, the doses for nonfruit fly pests were established based on information from studies in Japan and Hawaii on a limited number of species within each taxa (Follett and Armstrong 2004). This was the first time USDA-APHIS recommended a generic irradiation dose for any group of insects, albeit on a limited scale and only for certain Hawaii fruits. New Zealand is preparing a rule to allow import of tropical fruits from Australia using generic irradiation treatments of 150 Gy for fruit flies, 250 Gy for other insects, and 300 Gy for mites (Corcoran and Waddell 2003). Broad application of the generic irradiation concept to other taxa at the family or order level would be beneficial to promote trade in agricultural commodities and provide a treatment alternative for infested consignments arriving in importing countries. An International Database of Insect Disinfestation and Sterilization (IDIDAS 2003) under development by the International Atomic Energy Agency contains information on many Coleoptera (79 species, mainly curculionids) and Lepidoptera (72 species, mainly pyralids and tortricids); however, the majority of the studies referenced were not designed for quarantine purposes and lack the necessary large-scale tests. Information for other important regulatory arthropod groups such as Thysanoptera, Hemiptera, and Acari is limited. The “high-dose” approach is a variation of the generic dose concept.

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With this approach, a dose is set in excess of that believed to be required to control the pests associated with the commodity. For example, sweet potato growers in Hawaii are unable to ship sweet potatoes to California and the U.S. mainland without a quarantine treatment because of the presence of three regulatory pests, West Indian sweet potato weevil, Euscepes postfasciatus (Coleoptera: Curculionidae), sweet potato vine borer, Omphisa anastomosalis (Lepidoptera: Pyralidae), and sweet potato weevil, Cylas formicarius elegantulus (Coleoptera: Curculionidae). An irradiation treatment of 400 Gy for sweet potatoes was approved based on preliminary data for the pests (Follett 2003) and data from IDIDAS and the irradiation literature on curculionid and pyralid pests suggesting this dose would be adequate.This provisional irradiation treatment was published as a final rule in the Federal Register on February 18, 2004 (Federal Register 2004). This was the first time APHIS considered the high-dose approach for controlling a pest complex before research is completed to confirm a lower dose. Before generic treatments can be recommended for a wider range of insects and on a broader scale, information from coordinated research projects and large-scale tests is needed on effective irradiation doses for key pests and under-represented taxa. The most radiotolerant insect species tested to date is the Angoumois grain moth, which successfully reproduced at 500 Gy but not at 600 Gy (Ignatowicz 2004).Theoretically, this dose could be set as a generic treatment for all insects; however, a limiting factor for the practical use of a generic treatment at 600 Gy is the 1,000 Gy (1 kGy) maximum allowed dose for fresh produce set by the Food and Drug Administration.With typical dose uniformity ratios of 1.5–3.0 at commercial irradiation facilities, treatment to achieve a minimum absorbed dose of 600 Gy without exceeding 1 kGy would be difficult. Also, doses above 600 Gy adversely affect the organoleptic properties of many fresh fruits and vegetables (Kader 1986; Morris and Jessup 1994).A generic irradiation dose of 400 Gy for arthropods is supported by available data of Lepidoptera pupae and adults, and mites are excluded.

Regulatory Aspects of Irradiation The establishment of national regulations for the use of irradiation as a phytosanitary treatment began in 1930 with a failed proposal to use Xrays for treating fruit exported from Formosa (Koidsumi 1930). Seven decades later, the International Plant Protection Convention (IPPC) adopted an international standard for the use of irradiation as a phytosanitary treatment (IPPC 2003a).The evolution of irradiation as a phytosani-

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tary treatment from its disappointing start to international success was marked by a long history of national, regional, and international initiatives and several watershed events (discussed below), including the official acceptance of irradiation as a “safe” treatment and the establishment of a regulatory and policy framework by the United States for the implementation of irradiation as a phytosanitary treatment. Codex Alimentarius (Codex), the international organization responsible for establishing harmonized standards for food safety, adopted its Codex General Standard for Irradiated Food (CAC/RS 106-1979) in 1979. Although the standard does not specifically apply to phytosanitary treatments, it was the first international standard for irradiated food, and many phytosanitary treatments are for food commodities. The standard was subsequently revised in 1983 following the recommendations of the joint FAO-IAEA-WHO Expert Committee, and again in 2003 based on additional research indicating that the maximum absorbed dose could exceed 10 kGy when necessary to achieve a legitimate technological purpose (Codex 2003). Associated with the General Standard is the Codex Recommended International Code of Practice for the Operation of Irradiation Facilities. This was significant because it represented the first internationally harmonized guidelines on how to measure absorbed dose. It also describes relevant parameters in facilities; dosimetry and process control; good radiation processing practice; and product and inventory control (Codex 1984). The Code includes two annexes:Annex A is related to dosimetry, indicating how to calculate the overall average adsorbed dose and explaining the concept of limiting dose values, routine dosimetry, and process control;Annex B gives some examples of technological conditions for the irradiation of certain items. Mango is one of the examples. It is noted that mangoes may be irradiated for three objectives: (1) control of insects, (2) to improve quality (extend shelf life), and (3) to reduce microbial load using up to 1 kGy as an average dose. It is significant that the Code focused on mangoes because the chemical treatment of mangoes became a serious political issue in 1982 after the U.S. Environmental Protection Agency (EPA) announced a ban on the use of ethylene dibromide (EDB) because it was demonstrated to be a carcinogen (Ruckelshaus 1984). EDB was popular and widely used as a phytosanitary treatment at the time. The ban forced phytosanitary officials to seek alternative treatments for many commodities that were routinely treated for import and export, especially tropical fruits. Political pressures and growing interest in the commercialization of irradiation for the treatment of food in the United States spurred the

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Food and Drug Administration (FDA) to open the regulatory door in 1986 by publishing 21 CFR 179.26, “Irradiation in the Production, Processing and Handling of Food.” Among other things, this regulation authorized the use of irradiation up to 1 kGy for the disinfestation of arthropod pests in food, the use of up to 8 kGy for the control of microbial pathogens on seeds for sprouting, and up to 30 kGy for the microbial disinfestation of spices.This rule cleared the regulatory path for the USDA to authorize irradiation as a phytosanitary treatment on commodities for consumption. European authorities have historically been among the most reluctant to accept irradiation as a treatment for foods, but also among the most active in supporting research on the safety of irradiation. Concerns are principally focused on health risks to food processing workers, possible long-term effects of consuming irradiated food (especially for children), and fears that food producers and processors will be less motivated to use good manufacturing practice to ensure the wholesomeness of food if they are able to rely on irradiation treatment to produce clean products.A very limited list of herbs, spices, and seasonings is currently authorized from approved facilities with mandatory labeling requirements. In 2001, the European Commission suggested that this list be considered complete and recommended further research on the effects of consuming irradiated food and identifying alternative treatments rather than expanding the possibilities for irradiation (European Commission 2001). A similar situation occurs with Japan, where the use of nuclear technologies of any kind is perhaps more sensitive than for other countries for historical reasons.As do the Europeans, the Japanese allow and use irradiation for the treatment of food on a very limited and highly restricted basis.To date, the only phytosanitary treatment reported by Japan is for potatoes. A small proportion of Japan’s potato production is treated for sprout inhibition (Furuta 2004).

USDA Regulations The USDA had decided as early as 1966 that 150 Gy was the minimum dose to prevent adult emergence of three fruit flies: oriental fruit fly, Bactrocera dorsalis; Mediterranean fruit fly, Ceratitis capitata; and melon fruit fly, Bactrocera curcubitae; associated with papaya from Hawaii (Balock et al. 1966). In 1989, soon after FDA’s regulations went into effect, the Animal and Plant Health Inspection Service (APHIS), the USDA agency responsible for promulgating regulations dealing with quarantine treat-

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ments, published the first rule to allow the use of irradiation as a phytosanitary treatment.The rule specified a treatment of 150 Gy in order to ship fresh papaya from Hawaii to the mainland, Guam, Puerto Rico, and the Virgin Islands (Hawaii was later changed to 250 Gy). Despite being limited to a specific commodity, origin, and domestic program (and despite the fact that no fruit was immediately shipped due to the lack of a treatment facility in Hawaii), this minor domestic regulation had major global impacts as a result of the regulatory and policy implications it represented for the phytosanitary community. By publication of this rule, the United States made clear its acceptance of irradiation as both a safe and effective phytosanitary treatment and, for the first time, APHIS approved a treatment that dealt with a complex of pests (fruit flies) rather than a single pest.At the same time,APHIS recognized the legitimacy of a nonmortality treatment (the required response was “inability to fly”) and the possibility of detecting and accepting “live” quarantine pests in treated shipments (USDA-APHIS 1989). Regulatory interest in irradiation peaked again in 1992 when the fumigant methyl bromide (MB) was listed in the Montreal Protocol as one of the substances that causes depletion of the ozone layer. The Montreal Protocol is an international treaty for the regulation of ozone-depleting substances in the atmosphere (EPA 1993). At the Meeting of the Parties to the Montreal Protocol held September 1997 in Montreal, Canada, it was agreed that the production of MB should be phased out by a certain percentage each year beginning in 1999. Developed countries were expected to phase it out completely by 2005 and developing countries by 2015 (EPA 1996). Although the Montreal Protocol makes an exception for the use of MB as a quarantine treatment, the overall reduction in production of the fumigant over time has caused cost increases and reduced the availability of the compound with the net effect of making it increasingly less practical.The effect is not as immediate as was the ban on EDB, but the repercussions are just as significant because MB is also popular and widely used as a phytosanitary treatment for both food and nonfood items (for example, cut flowers and wood products). After 1995, rapidly increasing global trade pressures and the possible loss of methyl bromide as a fumigant for regulatory pest treatments made it imperative for practical treatment options to be explored. Unfortunately, the perception of public reluctance to accept irradiation and the relatively high initial costs associated with changing to irradiation as a preferred treatment technology made it less desirable than lower-cost alternatives.At the same time, technological advances, greater experience, and a growing body of research indicated that irradiation had increas-

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ingly greater potential as a treatment, or as an alternative treatment, for many quarantine pest problems. It is in this light that APHIS decided in 1996 to expand its regulatory framework addressing irradiation treatment, develop comprehensive policy statements, and begin encouraging international harmonization while also updating its own treatments and approving new ones. In a Policy Notice of 1996 titled “The Application of Irradiation to Phytosanitary Problems,”APHIS listed key positions and procedures, defined terms, offered research protocols, and proposed generic doses for nine fruit fly pests (USDA-APHIS 1996). In response to a petition from Hawaii, APHIS further expanded its authorization in 1997 to add the possibility of treating fresh papaya, lychees, and carambolas from Hawaii at 250 Gy (Moy and Wong 2002).An irradiation dose of 250 Gy rather than 150 Gy was established after review of the data in Seo et al. (1973). Following this,APHIS also approved the irradiation of sweet potato (Follett, in press) and other commodities from Hawaii. Fruits and vegetables from Hawaii that are currently authorized for irradiation treatment include abiu, atemoya, bell pepper, carambola, litchi, longan, eggplant, mango, papaya, pineapple (other than smooth Cayenne), rambutan, sapodilla, Italian squash, sweet potato, and tomato (Federal Register 2002; Follett 2004). Consistent with its Policy Notice, APHIS supplemented its authorizations for exports from Hawaii with regulations to also allow foreign imports by publishing a rule on Irradiation as a Phytosanitary Treatment for Imported Fresh Fruits and Vegetables (7 CFR 319.305). This regulation sets out specific standards for irradiation treatment to provide protection against 11 species of fruit flies and the mango seed weevil. Included also in this regulation are provisions that require the exporting country to establish Framework Equivalency Work Plans with APHIS demonstrating that the exporting country accepts irradiated commodities for import. Current plans are to continue expanding regulatory authorizations for the use of irradiation as a phytosanitary treatment based on additional research and experience (Pers. Comm 2005). Data currently under review offers possibilities for significant refinement of existing treatments and would make some new treatments available, including doses of 150 Gy for all tephritid fruit flies (Follett and Armstrong 2004), 300 Gy for the false red spider mite (Brevipalpus chilensis), 200 Gy for codling moth (Cydia pomonella), 250 Gy for koa seedworm (Cryptophlebia illepida), 250 Gy for litchi fruit moth (Cryptophlebia ombrodelta), 200 Gy for oriental fruit moth (Grapholita molesta), 92 Gy for plum curculio (Conotrachelus nenaphur), and 150 Gy for sweet potato weevil (Cylas formicarius elegantulus).

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Regional and International Harmonization The North American Plant Protection Organization (NAPPO), the regional organization responsible for setting phytosanitary standards recognized under the North American Free Trade Agreement (NAFTA), formally recognized the effectiveness of irradiation as a broad-spectrum quarantine treatment for fresh fruits and vegetables in 1989. In addition to NAPPO, other regional plant protection organizations that operate within the framework of the IPPC, including the European and Mediterranean Plant Protection Organization (EPPO), the Asia and the Pacific Plant Protection Commission (APPPC), the Comite de Sanidad Vegetal del Cono Sur (COSAVE), and the Organismo Internacional Regional de Sanidad Agropecuaria (OIRSA), endorsed irradiation as a quarantine treatment for fresh horticultural products at the Technical Consultation of Regional Plant Protection Organizations held in San Salvador in 1992 (FAO 1992). At the NAPPO Annual Meeting in 1994, a roundtable discussion was organized on “The Application of Irradiation to Phytosanitary Problems.” NAPPO delegates from Canada, Mexico, and the United States provided enough encouragement for the NAPPO Executive Committee to agree on an initiative to elaborate a regional standard.The policies put forward by APHIS in 1996 provided the framework for the development of “Guidelines for the Use of Irradiation as a Phytosanitary Treatment” that was adopted as a NAPPO standard (NAPPO 1997).This marked a significant step forward in international harmonization and became the springboard for creation of an international standard (IPPC 2003a). Since 1993, the IPPC has prepared international standards for phytosanitary measures designed to promote international harmonization and facilitate safe trade by avoiding the use of unjustified measures as barriers. Standards adopted by the IPPC must be observed by members of the World Trade Organization according to the Agreement on the Application of Sanitary and Phytosanitary Measures (the WTO-SPS Agreement). Governments must provide a technical justification (generally a risk assessment) for measures that are inconsistent with international standard or for measures put in place in the absence of a standard (WHO 1994). The Interim Commission on Phytosanitary Measures (ICPM), governing body of the IPPC, considered the global application of irradiation as a phytosanitary measure at its Third Session in 2001.A decision was made to create a working group with the purpose of developing an international standard for irradiation as a phytosanitary treatment, which was officially adopted in April 2003 (IPPC 2001; IPPC 2003b).The IPPC standard (International Standards for Phytosanitary Measures [ISPM] No. 18 Guidelines for the use of irradiation as a phytosanitary measure) describes

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specific procedures for the application of ionizing radiation as a phytosanitary treatment for regulated pests or articles. The document is organized like other IPPC standards, with sections including an introduction, scope, references, definitions and abbreviations, and an outline of requirements preceding the general and technical requirements. In addition, the standard includes an appendix providing scientific information on absorbed dose ranges for certain pest groups and another appendix providing guidance on undertaking research to develop irradiation treatments for regulated pests (IPPC 2003a).

Trade The establishment of the NAPPO standard in 1997 opened new possibilities for the use of irradiation in trade between Mexico and the United States. Mexico has great potential because of the high volume of fruit and vegetable exports requiring phytosanitary treatments. Mexico also has trained personnel and significant experience with irradiation treatments. What may be more important is that Mexico already has a regulatory framework in place for sanitary and phytosanitary treatments that allow food to be irradiated for consumption and for importation (Verdejo 1997). In 1998, a meeting was organized in Mexico to evaluate the capability of the country to initiate export markets for irradiated fruits and vegetables.Although it was recognized that Mexico had substantial potential for the export of irradiated fruits, especially mango, the producers opted instead to continue with treatments such as hot water dip that required a much lower initial investment in equipment and had no controversial implications for consumers. This attitude is changing, and Mexico is currently engaged in constructing new irradiation treatment facilities and pursuing necessary agreements with APHIS for the export of irradiated foods (Pers. Comm. 2004). The United States has opened the door for shipments of irradiated commodities from not only Mexico but also all countries. Several countries, including Brazil, Colombia, and Thailand, are pursuing Framework Equivalency Work Plans with APHIS in order to initiate bilateral trade in products irradiated for phytosanitary purposes (Pers. Comm. 2005). Based on the progressive regulatory directions established by the United States after 1980, many countries began to also consider legislation or regulations for irradiated food. Approximately 40 countries currently have regulations pertaining to irradiation as a treatment for food products and are treating or accepting treatment for at least one irradi-

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ated commodity (see Table 9.3). Although a large number of countries have approved irradiation as a treatment for food, few have large-scale commercial operations.This is due partly to regulatory barriers and partly to the lack of facilities and markets. Also, ensuring adequate throughput can be a substantial challenge given the seasonality of many agricultural products. The situation is slightly less complicated with nonfood treatments. Commodities such as wood products, cut flowers, and bird seed that may also require phytosanitary treatments are not subject to the same degree of regulation associated with food products.As a result, regulatory frameTable 9.3. Countries

Foods and Food Products Authorized for Irradiation for Selected

Country Algeria Argentina Australia

Bangladesh Belgium Brazil Canada Czech Republic Chile China

Croatia Cuba Denmark Ecuador Egypt Finland

Examples of Food Products Authorized or Treated with Irradiation Potatoes Spices and dried vegetables, garlic, egg products, and dehydrated bovine serum Breadfruit, carambola, custard apple, longan, litchi, mango, mangosteen, papaya and rambutan, herbs, spices, and herbal infusions Potatoes, onions, dried fish Feed for laboratory animals, spices, frozen frog legs, shrimp, aromatic herbs and teas, dehydrated vegetables Spices, dehydrated vegetables, fruits, vegetables, grain Potatoes, onions, wheat flour and whole wheat flour, spices and dehydrated seasonings, mango Spices Spices and condiments, dried vegetables, frozen food, potatoes, poultry meat Spices, pepper, condiments and seasoning, dried fruits, nuts and preserved fruit, cooked meat foods of livestock and poultry, fresh fruits and vegetables, frozen packaged meat of livestock and poultry, grains, beans and bean products, garlic spice, dehydrated vegetables, others Various tea herbs, chamomile, mixed spices, dry cauliflower and broccoli, paprika, liquid egg yolk, dry beef noodles Potatoes, onions, beans Spices Banana flour, spices, animal feed, raw jelly, honey, tea herbs Fresh bulbs, tuber crops, dried garlic, dried onion, herbs and spices Spices (continued)

Table 9.3. Foods and Food Products Authorized for Irradiation for Selected Countries (continued) Country

Examples of Food Products Authorized or Treated with Irradiation

France

Laboratory animal food, spices,Arabic gum, dehydrated vegetables, cereal, poultry (frozen de-boned chicken), frog legs, shrimp, dried fruit and vegetables, rice flour, strawberries, bovine serum Germany Spices Ghana Yam, maize Hungary Spices, onions, wine cork, enzymes India Pulses, dried seafood, fresh seafood, frozen seafood, spices and dry vegetables, seasonings Indonesia Frozen seafood products (including frog legs), cacao powder, spices, food packaging, rice Iran Spices, dried fruits, nuts Iraq Spices Israel Spices, condiments, dry ingredients Italy Spices Japan Potato Republic of Korea Potato, onions, garlic, chestnuts, mushrooms (fresh and dried), spices, dried meat, red pepper, paste powder, soy sauce powder, starch for condiments, dried vegetables, yeast-enzyme products, aloe powder, ginseng products, mushrooms (fresh & dried), spices, dried meat, shellfish powder, soybean paste powder, starch for condiments, dried vegetables, dried yeast and enzyme products, aloe powder, ginseng products, sterile meals Malaysia Spices Mexico Spices, dried vegetables, chili, dried meat Moroco Spices Netherlands Spices, frozen products, poultry, dehydrated vegetables, egg powder, packaging material New Zealand Breadfruit, carambola, custard apple, longan, litchi, mango, mangosteen, papaya, rambutan, herbs, spices and herbal infusions Norway Spices Pakistan Potatoes Peru Spices, condiments, dehydrated products, medical herbs, flours, food supplements Philippines Spices (onion powder, garlic powder, cayenne powder, ground black pepper, Spanish paprika, dehydrated chives, ground anise, instant gravy, sausage seasoning, minced onion), frozen fruits (avocado, mango, macapuno, durian, ube, atis, buco, cheese, fruit cocktail), Solo papaya, Carabao mango, Cavendish banana

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163

Table 9.3. Foods and Food Products Authorized for Irradiation for Selected Countries (continued) Country Poland Portugal South Africa

Syria Thailand Turkey

Ukraine United Kingdom United States Vietnam Yugoslavia

Examples of Food Products Authorized or Treated with Irradiation Spices, dried mushrooms, medical herbs Spices Cereal, dairy products, dehydrated foods, dehydrated vegetables, dried fruit, egg products, fish, fresh vegetables, garlic, health preparations, honey products, marinade, royal jelly, shelf-stable foods, soya mixtures, spices and herbs,Torulite yeast, vegetable powder Chicken, cocoa beans, condiments, dates, fresh fish, dried fish products, mango, onions, licorice, spices Fermented pork sausage, sweet tamarind, spices, onions, enzymes Spices, dried seasonings and herbs, dried vegetables, meat and meat products, frozen fish and seafood, frozen frog legs, dried fruits Spices Spices Spices, chicken, beef, fish, fresh fruits and vegetables, meals Spices Spices

Source: ICGFI, 1997–2002; Loaharanu, 1997

works for these treatments do not address health and safety concerns but rather emphasize the efficacy of the treatment, and the integrity of the treatment process and facility. The evolution of regulatory frameworks for the adoption and implementation of irradiation as a phytosanitary treatment has been marked by numerous successes around the world. In the past, regulatory uncertainties have heightened anxiety among investors and producers who were already concerned about potential problems with public acceptance despite extensive information about the safety and effectiveness of irradiation.Today, the world has an international standard as a global reference point for the use of irradiation as a phytosanitary treatment, and the United States has put in place a regulatory framework demonstrating full acceptance of the technology.The uncertainties associated with potential regulatory barriers are substantially reduced, and the path is clear to realizing the full potential of irradiation as a phytosanitary treatment.

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References Ahmed M. 2001. Infestation of stored grains, pulses, dried fruits and nuts, and other dried foods. p. 77–112. In: Food Irradiation: Principles and Applications, RA Molins, ed. John Wiley & Sons, Inc., New York. Alpen, EN. 1998. Radiation Biophysics.Academic Press, San Diego, CA. Baker,AC. 1939.The basis for treatment of products where fruit flies are involved as a condition for entry into the United States. U.S. Department of Agriculture Circular No. 551. Baker RT, Cowley JM, Harte DS, Frampton ER. 1990. Development of a maximum pest limit for fruit flies (Diptera: Tephritidae) in produce imported into New Zealand. J Econ Entomol 83:13–17. Balock, JW, Burditt AK Jr., Christenson LD. 1966. Effects of gamma radiation on various stages of three fruit fly species. J Econ Entomol 56:42–46. Batchelor TA. 1989. Potential use of biochemical data in the development of radiationbased insect disinfestations treatments for fresh commodities. PhD dissertation, University of California, Davis , CA. Burditt,AK. 1994. Irradiation, p. 101–117. In: J. L. Sharp and G. J. Hallman, eds., Quarantine Treatments for Pests of Food Plants.Westview Press, Boulder, Colorado. Burditt,AK. 1996. Irradiation as a quarantine treatment against fruit flies. p. 479–484. In: B. McPheron and G. Steck, eds., Fruit Fly Pests: A World Assessment of their Biology and Management. St. Lucie Press, Delray Beach, Florida. Bustos ME, Enkerlin W, Reyes J,Toledo J. 2004. Irradiation of mangoes as a postharvest treatment for fruit flies (Diptera:Tephritidae). J Econ Entomol 97:286–292. Castro D, Espinosa DJ,Vargas M. 2004. Ionizing radiation as a quarantine treatment for controlling Brevipalpus chilensis (Acarina:Tenuipalpidae) in Thompson seedless grapes, p. 143–53. In: Irradiation as a Phytosanitary Treatment of Food and Agricultural Commodities. IAEA Techdoc 1427,Vienna,Austria. Codex. 1984. Codex Recommended International Code of Practice for the Operation of Radiation Facilities used for the Treatment of Foods (CAC/RCP 10-1979, Rev 1). Codex Alimentarius Commission,Vol. XV, Geneva. Codex. 2003. Codex General Standard for Irradiated Foods, Codex Stan 106-1983, Rev. 12003. Codex Alimentarius Commission. FAO, Rome. Corcoran RJ,Waddell BC. 2003. Ionizing Energy Treatments for Quarantine Disinfestation. Horticulture Australia Limited. Couey HM, Chew V. 1986. Confidence limits and sample size in quarantine research. J Econ Entomol 79:887–890. Diehl JF. 2001. Achievements in Food Irradiation during the 20th Century, p. 1–7. In: Irradiation for Food Safety and Quality, P. Loaharanu and P.H.Thomas, eds. Proceedings of FAO/IAEA/WHO International Conference on Ensuring the Safety and Quality of Food through Radiation Processing.Technomic Publishing, Lancaster, PA. Ducoff HS. 1972. Causes of cell death in irradiated adult insects. Biol Rev 47:211240. EPA. 1993. Protection of Stratospheric Ozone: Final Rule. Federal Register 58 (236): 65018–65082. EPA. 1996. Revocation of Pesticide Food Additive Regulations: Final Rule. Federal Register 61 (57):11994–11999. European Commission. 2001. Commission communication on foods and food ingredients authorized for treatment with ionizing radiation in the Community [COM (2001) 4722002/2008 (COS)]. European Commission, Brussels.

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European Commission. 2002. Statement of the Scientific Committee on Food on a Report on 2-alkylcyclobutanone (expressed on 3 July 2002), SCF/CS/NF/IRR/26 ADD 3 Final. European Commission, Brussels. European Parliament. 2002. Motion for a Resolution, European Parliament resolution on the Commission communication on foods and food ingredients authorized for treatment with ionizing radiation in the Community [COM (2001) 472-C5-2002/00102002/2008) (COS)]. European Parliament, Brussels. Federal Register. 1997. Papaya, carambola, and litchi from Hawaii. 62(132):36967–36976, July 10, 1997, Rules and Regulations. Federal Register. 2002. Fruits and vegetables from Hawaii. 67 (99): 35932-35936, May 22, 2002. Rules and Regulations. Federal Register. 2004. Irradiation of sweetpotatoes from Hawaii. 69(32):7541–7547, February 18, 2004, Rules and Regulations. Food and Agriculture Organization (FAO). 1992. Report of the Fourth Technical Consultation Among Regional Plant Protection Organizations, San Salvador, El Salvador, 11–15 May 1992.AGPP/1992/M/3. FAO, Rome. Fisher K. 1997. Irradiation effects in air and in nitrogen on Mediterranean fruit fly (Diptera: Tephritidae) pupae in Western Australia. J Econ Entomol 90:1609–1614. Follett PA. 2002. Irradiation as a quarantine treatment for mango seed weevil (Coleoptera: Curculionidae). Proc Hawaiian Entomol Soc 35:95–100. Follett PA. 2004. Irradiation to control insects in fruits and vegetables for export from Hawaii. Rad Phys Chem 71:161–4. Follett PA. 2004. Generic vapor heat treatment to control Maconellicoccus hirsutus. J Econ Entomol 97:1263–1268. Follett PA. In press. Irradiation as a methyl bromide alternative for postharvest control of Omphisa anastomosalis (Lepidoptera: Pyralidae), Euscepes postfasciatus and Cylas formicarius elegantulus (Coleoptera: Curculionidae) in sweetpotatoes. J Econ Entomol. Follett PA, Lower R. 2000. Irradiation to ensure quarantine security for Cryptophlebia spp. (Lepidoptera: Tortricidae) in sapindaceous fruits from Hawaii. J Econ Entomol 93: 1848–1854. Follett PA, Gabbard Z. 2000. Effect of mango weevil (Coleoptera: Curculionidae) damage on mango seed viability. J Econ Entomol 93:1237–1240. Follett PA, McQuate GT. 2001. Accelerated development of quarantine treatments for insects on poor hosts. J Econ Entomol 94:1005–1011. Follett PA. 2003. Irradiation as a methyl bromide alternative for sweetpotato exports from Hawaii. In: Proc.Annual International Conference on Methyl Bromide Alternatives and Emissions Reductions, San Diego, CA. (http://mbao.org/2003/) Follett PA, Sanxter SS. 2003. Lychee quality after hot-water immersion and x-ray irradiation quarantine treatments. HortScience 38:1159–1162. Follett PA, Armstrong JW. 2004. Revised irradiation doses to control melon fly, Mediterranean fruit fly and oriental fruit fly (Diptera:Tephritidae) and a generic dose for tephritid fruit flies. J Econ Entomol 97:1254–1262. Follett PA, Neven LG. 2006. Current trends in quarantine entomology. Annu Rev Entomol 51: 359–385. Furuta, M. 2004. Current status of information transfer activity on food irradiation and consumer attitudes in Japan. Rad Phys Chem 71:501–504. Gould WP, von Windeguth DL. 1991. Gamma irradiation as a quarantine treatment for carambolas infested with Caribbean fruit flies. Fla Entomol 74:297–300.

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Hallman GJ. 1998. Ionizing radiation quarantine treatments. An Soc Entomol Brasil 27: 313–323. Hallman GJ. 2001. Irradiation as a quarantine treatment. P. 113–130. In: Food Irradiation: Principles and Applications, R. Molins, ed. John Wiley & Sons, New York. Hallman GJ. 2003. Ionizing irradiation quarantine treatment against plum curculio (Coleoptera: Curculionidae). J Econ Entomol 96:1399–1404. Hallman GJ. 2004. Ionizing irradiation quarantine treatment against oriental fruit moth (Lepidoptera: Tortricidae) in ambient and hypoxic atmospheres. J Econ Entomol 97:824–827. Hallman GJ. 2004. Irradiation disinfestation of apple maggot (Diptera: Tephritidae) in hypoxic and low-temperature storage. J Econ Entomol 97:1245–1248. Hallman GJ, Martinez LR. 2001. Ionizing irradiation quarantine treatment against Mexican fruit fly in citrus. Postharvest Biol Technol 23:71–77. Hallman GJ, Loaharanu P. 2002. Generic ionizing radiation quarantine treatments against fruit flies (Diptera:Tephritidae) proposed. J Econ Entomol 95:893–901. Hara AH,Yalemar JA, Jang EB, Moy JH. 2002. Irradiation as a possible quarantine treatment for green scale Coccus viridis (Green) (Homoptera: Coccidae). Postharvest Biol Technol 25:349–358. Heather NW. 1992. Review of irradiation as a quarantine treatment for insects other than fruit flies. P. 203–18. In: Use of irradiation as a quarantine treatment of food and agricultural commodities. International Atomic energy Agency,Vienna,Austria. Heather NW. 2004. Generalized quarantine disinfestation research protocol. P. 171–178. In: Irradiation as a Phytosanitary Treatment of Food and Agricultural Commodities. IAEA Techdoc 1427,Vienna,Austria. Heather NW, Corcoran RJ, Banos C. 1991. Disinfestation of mangoes with gamma irradiation against two Australian fruit flies. J Econ Entomol 84:1304–1307. IDIDAS. 2003. International Database on Insect Disinfestation and Sterilization. Web site: www-ididas.ieae.org/ididas/. International Atomic Energy Agency,Vienna. ICGFI (International Consultative Group on Food Irradiation). 1991. Irradiation as a quarantine treatment of fresh fruits and vegetables. ICGFI Document No. 13. International Atomic Energy Agency,Vienna,Austria. ICGFI 1997–2002. Status Reports on Food Irradiation by Member Countries of the International Consultative Group on Food Irradiation (ICGFI) 1997–2002. International Atomic Energy Agency,Vienna. Ignatowicz S. 2004. Irradiation as an alternative to methyl bromide fumigation of agricultural commodities infested with quarantine stored product pests. P. 51–66. In: Irradiation as a Phytosanitary Treatment of Food and Agricultural Commodities. IAEA Techdoc 1427,Vienna,Austria International Plant Protection Convention (IPPC). 2001. Report of the Third Session of the Interim Commission on Phytosanitary Measures.April, 2001. FAO, Rome. International Plant Protection Convention (IPPC). 2003a. International Standards for Phytosanitary Measures (ISPM) No. 18, Guidelines for the use of irradiation as a phytosanitary measure.April. 2003. FAO, Rome. International Plant Protection Convention (IPPC). 2003b. Report of the Fifth Session of the Interim Commission on Phytosanitary Measures.April, 2003. FAO, Rome. Jang, EB, Moffitt H. 1994. Systems approaches to achieving quarantine security. P. 225–237. In: J. L. Sharp and G. J. Hallman, eds., Quarantine Treatments for Pests of Food Plants. Westview Press, Boulder, Colorado. Kader, AA. 1986. Potential applications of ionizing radiation in postharvest handling of fresh fruits and vegetables. Food Technol 40:117–121.

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Kaneshiro, KY, Ohta AT, Kurihara JS, Kanegawa KM, Nagamine LR. 1985. Gammaradiation treatment for disinfestations of the medfly in thirty-five varieties of California-grown fruits. P. 98–110. In: J. Moy, ed., Radiation Disinfestation of Food and Agricultural Products. Hawaii Institute for Tropical Agriculture and Human Resources, Honolulu, HI. Koidsumi K. 1930. Qualitative studies on the lethal actions of X rays upon certain insects. J Soc Trop Agric Taiwan 7:243. Komson, P, Smitasiri E, Lapasatukul C, Unahawutti U, Nonthachai S, Sukkaseam S,Tantidham K, Sutantawong M. 1992. Use of radiation in an export plant quarantine programme. P. 117–132. In: Use of irradiation as quarantine treatment of food and agricultural commodities. International Atomic Energy Agency,Vienna,Austria. Koval, TM. 1994. Intrinsic stress resistance of cultured lepidopteran cells. P. 157–185. In: Insect Cell Biotechnology, K. Marmarorosh and A. McIntosh, eds. CRC Press, Boca Raton, Florida, U.S.A. Landolt PJ, Chambers DL, Chew V. 1984.Alternative to the use of probit 9 mortality as a criterion for quarantine treatments of fruit fly (Diptera:Tephritidae) infested fruit. J Econ Entomol 77:285–287. Loaharanu P. 1997.“International Developments of Food Irradiation,” Memorias Seminario Nacional, Aceptacion y Comercio de Alimentos Irradiados. 27–29 October, 1997. Instituto Nacional de Investigaciones Nucleares.Toluca, Mexico, p. 1–8. Mangan, RL, Frampton ER,Thomas DB, Moreno DS. 1997.Application of the maximum pest limit concept to quarantine security standards for the Mexican fruit fly (Diptera: Tephritidae). J Econ Entomol 90:1433–1440. Mansour M, Mohamad F. 2004. Gamma irradiation as a phytosanitary measure for exported Syrian fresh fruit. p. 19–36. In: Irradiation as a Phytosanitary Treatment of Food and Agricultural Commodities. IAEA Techdoc 1427,Vienna. Morris SC, Jessup AJ. 1994. Irradiation. P. 163–190. In: R. E. Paull and J. W. Armstrong, eds., Insect Pests and Fresh Horticultural Products: Treatments and Responses. CAB International,Wallingford, UK. Moy JH, Wong L. 2002.The efficacy and progress in using radiation as a quarantine treatment of tropical fruits—a case study in Hawaii. Rad Phys Chem 63:397–401. NAPPO 1997. Guidelines for the Use of Irradiation as a Phytosanitary Treatment. NAPPO Regional Standard for Phytosanitary Measures (archive). NAPPO, Ottawa. Nation,JL, Burditt AK. 1994. Irradiation. P. 85–102. In: Insect Pests and Fresh Horticultural Products: Treatments and Responses. Paull, RE, Armstrong, JW eds. CAB International Wallingford, UK. Personal communication(s). 2005. Paul Gadh, Treatment Specialist with USDA-APHIS Plant Protection and Quarantine, Phytosanitary Issues Management Staff. Riverdale, MD. Personal communication. 2004. Dr. Javier Trujillo Arriaga, Director en Jefe, Servicio Nacional de Sanidad, Inocuidad y Calidad Agroalimentaria (SENASICA). May, 2004. Mexico City, Mexico. Powell, MR. 2003. Modeling the response of the Mediterranean fruit fly (Diptera: Tephritidae) to cold treatment. J. Econ Entomol 96:300–310. Rigney, CJ. 1989. Radiation-disinfestation of fresh fruit. P. 425–434. In:A. S. Robinson and G. Hooper, eds., World crop pests, 3B: Fruit Flies, their Biology, Natural Enemies, and Control, Elsevier,Amsterdam. Rigney CJ,Wills PA. 1985. Efficacy of gamma irradiation as a quarantine treatment against Queensland fruit fly. P. 116–120. In: Radiation disinfestations of food and agricultural products, J. H. Moy, ed. University of Hawaii at Manoa, Honolulu, Hawaii.

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Robertson JL, Preisler HK. 1992. Pesticide Bioassays with Arthropods. CRC Press, Boca Raton, Florida. Ruckelshaus WD. 1984. Ethylene dibromide, amendment of notice of intent to cancel registration of pesticide products containing ethylene. Federal Register 49: 14182–14185. Seo ST, Kobayashi RM, Chambers DL, Dollar DM, Hanaoka M. 1974. Hawaiian fruit flies in papaya, bell pepper, and eggplant: quarantine treatment with gamma irradiation. J Econ Entomol 66:937–939. Sproul AN. 1976. Disinfestation of Western Australian Granny Smith apples by cold treatment against the egg and larval stages of the Mediterranean fruit fly (Ceratitis capitata [Wied.]) Austral J Exp Agric Anim Husb 16:280–285. Tilton EW, Brower JH. 1983. Radiation effects on arthropods. P. 269-316. In: Preservation of Food by ionizing Radiation,Vol. 2, E.S. Josephson and M.S. Peterson, eds. pp. CRC Press Inc., Boca Raton, FL. Toledo J, Liedo P, Bustos EM. 2003. Gamma irradiation as a guava treatment for guavas infested with larvae of Anastrepha striata Schiner (Diptera: Tephritidae). Folia Entomologia Mexicana 42:371–379. USDA-APHIS. 1989. Use of irradiation as a quarantine treatment for fresh fruits of papaya from Hawaii. Federal Register 54(4):387–392. USDA-APHIS. 1996. The application of irradiation to phytosanitary problems (Notice of Policy). Federal Register 61(95):24433–24439. USDA-APHIS. 2002. Irradiation Phytosanitary Treatment of Imported Fruits and Vegetables Final Rule. Federal Register Vol. 67 No 205:65016–65029. Vail PV, Tebbetts JS, Mackey BE, Curtis CE. 1993. Quarantine treatments: a biological approach to decision making for selected hosts of codling moth (Lepidoptera: Tortricidae). J Econ Entomol 86:70–75. Verdejo S Maricela. 1997. Irradiacion de Alimentos, Legislacion Vigente. P. 133–137. In: Memorias Seminario Nacional,Aceptacion y Comercio de Alimentos Irradiados. 27–29 October, 1997. Instituto Nacional de Investigaciones Nucleares.Toluca, Mexico. Whyte CF, Baker RT, Cowley JM, Hart DS. 1994. A quantitative method for calculating the probability of pest establishment from imported plants and plant products, as a part of pest risk assessment. N. Z. Plant Protection Centre Publications No. 4, Auckland, New Zealand. WHO (World Health Organization). 1981. Wholesomeness of irradiated food. Technical Report Series No. 659.WHO. Geneva. WHO (World Health Organization). 1994. Agreement on the application of sanitary and phytosanitary measures. GATT Uruguay Round Agreements.World Trade Organization, Geneva.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 10 LOW-DOSE IRRADIATION OF FRESH AND FRESH-CUT PRODUCE: SAFETY, SENSORY,AND SHELF LIFE Brendan A. Niemira and Xuetong Fan

Introduction With consumption of fresh and fresh-cut produce increasing in the United States, and market globalization becoming a more important factor, has come greater concern over produce-associated foodborne illness (Thayer and Rajkowski 1999). From an epidemiological standpoint, foodborne illness outbreaks in the United States associated with contaminated fruits, vegetables, salads, and juices have risen from fewer than 20 throughout the 1970s to more than 100 in the 1990s (Sivapalasingam and others 2004). New tools to ensure the safety of fresh and fresh-cut produce are required; low-dose irradiation is one of the more promising of these. Vegetables were among the first experimental subjects in studies of physiological response to irradiation (Guilleminot 1908; Miege and Coupe 1914).The first studies with irradiated produce typically used relatively high doses and were intended to achieve reductions in spoilage bacteria and fungi equivalent to thermal pasteurization (Diehl 1995).This research helped to define sterilization doses for commensal and spoilage organisms. However, these doses frequently exceeded the maximum radiation tolerances of vegetable commodities tested, resulting in loss of quality (Howard and Buescher 1989; Prakash and others 2000b). For this reason, irradiation was historically regarded as less suited to application to produce (Maxie and Abdel-Kader 1966; Yu and others 1996; Osterholm and Potter 1997). However, more recent research with lower radiation 169

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doses, that is, less than 3 kiloGray (10 kGy = 1 Mrad), has suggested a role for irradiation as one of several “hurdles” in fruit and vegetable processing (Thayer and Rajkowski 1999; Smith and Pillai 2004; Niemira and Deschenes 2005).This approach is of particular value with regard to the elimination of human pathogens from produce.The role of contaminated produce in foodborne illness is a subject of increasing concern due to changes in consumption patterns associated with minimally processed fruits, vegetables, and juices (NACMCF 1999; Sivapalasingam and others 2004). It bears reiterating that foods treated with ionizing radiation have consistently been shown to be wholesome and nutritious (WHO 1999; Smith and Pillai 2004).

Produce Microbiology and Irradiation Treatment Phytopathogenic and human pathogenic bacteria may be internalized in fruits and vegetables, beyond the reach of surface sanitizers (Takeuchi and Frank 2000; Burnett and Beuchat 2002).The penetrability and subsurface antimicrobial efficacy of irradiation suggest that it can play an important role in the sanitization of produce. Of the three types of ionizing radiation commonly employed, electron beam (e-beam) is less penetrating than photon sources (x-rays or gamma rays), with maximal penetration of 6–7 cm for the former vs. 20–24 cm for the latter in foods of approximately unit density (1g/cc) (Niemira and Deschenes 2005). With either technology, irregular or asymmetric treatment results in uneven irradiation, with some parts of the product receiving a higher dose than others. Excessive variation in treatment can lead to undesirable sensory damage (dose too high) or lack of antimicrobial or phytosanitary efficacy (dose too low). Computer simulations suggest that, for irregularly shaped produce such as apples treated with the less penetrating e-beam, the ratio of the highest dose delivered to the lowest dose delivered (the Max/Min ratio) can be as high as 3.0 (Brescia and others 2003). It is thus readily shown that fruits and vegetables, with their irregular shapes and variations of density, present a complex challenge for effective, uniform treatment with e-beam irradiation. Fresh produce may be irradiated for a number of purposes, including inhibition of sprouting, delay of ripening, disinfestation (elimination or sterilization of insect pests), and reduction of microbial load. The doses required for effective reduction of microbial load (typically at least 0.5 kGy or greater) are higher than that required for the other major purposes (typically less than 0.3 kGy) and thus will exert the largest effect on produce quality and shelf life (Farkas and others 1997).The most im-

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portant effect of irradiation in the treatment of produce, therefore, is reduction of microbial load, with the intended target of the intervention either spoilage phytopathogens or contaminating human pathogens (Thayer and Rajkowski 1999; Niemira and Deschenes 2005).The primary means of preserving fresh produce in the supply chain connecting producer and consumer are refrigeration and modified atmosphere packaging (Sumner and Peters 1997; Niemira and others 2005). The nature of fresh produce, that is, living tissue that respires, metabolizes, ripens, and so forth, makes it relatively sensitive to ionizing radiation. Improper or excessive treatment can lead to changes in firmness, aroma, color or taste (Yu and others 1996; Mahrouz and others 2004) or delayed effects on phytoplane microbial ecology (Howard and Buescher 1989; Al-Kahtani and others 2000; Prakash and others 2000a). Irradiated fresh produce, as with all irradiated foods, must adhere to the basic rules of good manufacturing practice for preservation of quality and food safety. Fungi and viruses are typically more resistant to radiation than are bacteria. D10 values, that is, the amount of radiation necessary to achieve a 90% (1-log) reduction, are in the range of 1 to 3 kGy for fungi (Narvaiz and others 1992; El-Samahay and others 2000; Niemira and Deschenes 2005) and somewhat higher for viruses (Howard and Buescher 1989;Yu and others 1996; Monk and others 1994).The doses required to achieve meaningful population reductions of fungal and viral contaminants (that is, 3–5 log10) typically result in loss of sensorial quality of fresh and freshcut produce. Low-dose irradiation has been shown to suppress, but not eliminate, some phytopathogenic fungi responsible for storage losses (Niemira and Deschenes 2005). In contrast, the D10 for pathogenic bacteria on produce ranges from 0.2–0.8 kGy (Foley and others 2002; Niemira and others 2002; Niemira 2003; Martins and others 2004); this degree of sensitivity would allow a 5 log10 reduction with doses between 1 and 4 kGy, a more achievable level of treatment. Irradiation is therefore clearly best suited to control of bacterial pathogens, as opposed to viral or fungal pathogens.

Irradiation to Enhance Microbial Safety of Produce Fresh and fresh-cut produce have been implicated in instances of foodborne illness with increasing frequency in recent years (Sivapalasingam and others 2004). Methods to sanitize these products so as to improve their safety have been improving, but the physical nature of fruits and vegetables presents serious challenges to conventional means of removing or inactivating pathogenic bacteria. Plant parts such as leaves, stems,

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fruits, and roots typically support 103–106 colony-forming units (cfu) per gram of plant tissue (Sumner and Peters 1997; Mercier and Lindow 2000). Sanitization of produce has traditionally meant surface treatment; however, an improved understanding of how bacteria inhabit the surface and internal spaces of fruits and vegetables is resulting in new concerns over the efficacy of traditional antimicrobial measures. Internalization of Bacteria Bacteria have recently been shown to enter fruits and vegetables through natural openings such as stomata, stem scar, calyx, and so forth, or via abiotic wounds and/or phytopathogenic penetrations; once internalized, bacteria can survive within the produce for days or weeks (Takeuchi and Frank 2000; Riordan and others 2000). Bacteria may migrate naturally, or they may be drawn in with contaminated water by improper washing steps (Penteado and others 2004). Bacteria internalized within produce occupy cell junctions and intracellluar spaces at least 50 microns deep (Auty and others 2005) and are therefore beyond the reach of chemical sanitizers (Fett 2000; Niemira and others 2005). These require mechanisms that are more penetrating; although this has traditionally meant heat treatments (Gorny 2005), the heat-sensitive nature of fresh produce limits this approach and prompts examination of irradiation as an alternative. Biofilms The de facto life habitat for phytoplane bacteria is as a biofilm, a complex community of many bacterial species bound to the plant surface in a durable exopolysaccharide matrix (Carmichael and others 1999; Fett 2000). Human pathogens such as E. coli and Salmonella are known to form durable biofilms on industrial surfaces (Dewanti and Wong 1995; Korber and others 1997). Of concern for food safety, the protective nature of bacterial biofilms has been repeatedly demonstrated to reduce the efficacy of antimicrobial measures such as ozone, chlorine, and hydrogen peroxide, frequently by orders of magnitude (Stewart and others 2004). Unattached L. monocytogenes cells were reduced by 8.29 log10 cfu by treatment with 0.25 ppm ozone for 3 min.This treatment resulted in only a 1.48 log10 cfu reduction for biofilm-associated L. monocytogenes (Robbins and others 2005).That study showed that a 16⫻ concentration (4.00 ppm) was required to achieve comparable reductions for the biofilm (8.07 log10 cfu). In contrast, a recent study of three Salmonella isolates has shown that biofilm-associated bacteria are as sensitive as or

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more sensitive to irradiation than planktonic bacteria (Niemira and Solomon 2005).This finding suggests that the penetrating nature of ionizing radiation may make it uniquely suited to the problem of internalized, biofilm-associated, or otherwise protected pathogens on or in produce. Post-Irradiation Recovery and Regrowth As an antimicrobial process, the reduction of pathogen populations is the primary goal of irradiation; however, pathogen regrowth in storage following irradiation due to reduced interspecies competition is a known phenomenon. Palekar and others (2004) examined cut cantaloupe pieces and determined that a chlorine wash (200 ppm sodium hypochlorite) combined with e-beam irradiation to 1.4 kGy led to a lasting suppression of the aerobic microflora during the 21 d storage period. A lower radiation dose, or a treatment that used a water wash, led to significant regrowth of the microflora. On studies of inoculated endive leaves, L. monocytogenes was observed to regrow in storage following a dose equivalent to a 99% (2 log10) reduction, that is, 0.42kGy (Niemira and others 2003). After this moderate dose, the pathogen eventually regrew to equal or exceed the level seen in the untreated control. However, a higher dose of 0.84 kGy, calibrated to achieve a 4 log10 reduction, suppressed the pathogen throughout the 19 d of the storage period.A later study using modified atmosphere packaging (MAP) confirmed the capacity of L. monocytogenes to regrow after relatively mild doses of irradiation, sufficient to achieve 1-3 log10 reductions (Niemira and others 2004). A reduced-O2, enhanced-CO2 packaging scheme effectively suppressed this capacity and prevented the pathogen from regrowing. Treatment Parameters for Irradiation of Produce A dose of 1.0 kGy reduced total aerobic plate count and L. monocytogenes on pre-cut bell pepper by approximately 4 log10 cfu/g; storage (4 d) at abuse temperatures (10 or 15° C) led to regrowth, but refrigeration temperature (4° C) suppressed regrowth of the pathogen, preserving the initial efficacy of the treatment (Farkas and others 1997). E. coli and L. monocytogenes were effectively eliminated (>5 logs) from diced celery by 1.0 kGy (Prakash and others 2000b). Peeled, ready-to-use carrots that were treated with 1 kGy showed aerobic plate counts reduced by 4 log10 cfu when packed in air, and 4.5 log10 reduction when packed under modified atmosphere (Lafortune and others 2005).The use of an edible coating in combination with irradiation improved the keeping quality of the carrot pieces in that study.Total aerobic counts were reduced by ~3 logs

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on iceberg lettuce by 0.19 kGy (Hagenmaier and Baker 1997), by ~1.5 logs on romaine lettuce by 0.35 kGy (Prakash and others 2000a) and ~2 logs on shredded carrot by 0.45 kGy (Hagenmaier and Baker 1998) by irradiation and storage under MAP. Thus, it can readily be seen that optimized combinations of antimicrobial treatments will serve to improve the applicability of irradiation to a wider range of vegetable products. Rajkowski and Thayer (2000) obtained D10 values for E. coli O157:H7 of 0.34, 0.27 and 0.26 kGy on radish, alfalfa, and broccoli sprouts, respectively. D10 values obtained for Salmonella on radish sprouts in that study were dependent on the provenance of the isolates, that is, the type of food product from which they were derived: 0.54 kGy (meat sources) in contrast to 0.46 kGy (vegetable sources). D10 values obtained by Bari and others (2004) for cocktails of E. coli O157:H7 and Salmonella were approximately 0.3 kGy for both pathogens when tested on radish sprouts, roughly comparable to those of Rajkowski and Thayer (2000). However, when tested on mung bean sprouts, the D10 values of E. coli O157:H7 (0.18kGy) and Salmonella (0.16kGy) cocktails were markedly lower. Goularte and others (2004) obtained somewhat different D10 values on shredded iceberg lettuce for E. coli O157:H7 (~0.11 kGy) and Salmonella (~0.2 kGy).The sensitivity of the irradiation process to factors such as the provenance of the experimental isolate(s), the suspending medium, and treatment conditions indicates that, before irradiation can be implemented within any given commercial context, validation of the protocol using commercially applicable factors (dose, conditions, product, processing time, and so on) is a necessary step. Influence of Plant Variety The specific variety of fruit or vegetable has been shown to have a significant effect on the response to irradiation. This has been shown in regards to sensory responses, including loss of color, firmness, aroma, and so on, for a number of types of produce: iceberg lettuce (Hagenmaier and Baker 1997) as opposed to romaine lettuce (Prakash and others 2000a); the potato varieties Ajax vs. Diamant (Al-Kahtani and others 2000); and blueberry cultivars Climax (Miller and others 1994) vs. Sharpblue (Miller and others 1995) vs. Brightwell and Tifblue (Miller and McDonald 1996). The differences among varieties can also result in significant differences in the D10 for associated pathogens. A series of studies determined the D10 for E. coli O157:H7, Salmonella and L. monocytogenes on four lettuce varieties: red leaf, green leaf, Iceberg, and Boston. These studies found evidence for variety- and pathogen-specific influence on radiation sensitivity (Table 10.1).These complex and poorly understood factors in-

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Low-Dose Irradiation of Fresh and Fresh-Cut Produce Table 10.1.

Radiation D10 Values for Pathogens on Four Lettuce Varieties D10 values (kGy) on lettuce types1

Pathogen E. coli O157:H72 Salmonella3 L. monocytogenes3

Red leaf

Green leaf

Boston

Iceberg

0.119a 0.23a 0.19a

0.123a 0.31b 0.19a

0.140b 0.24a 0.19a

0.136b 0.25a 0.20a

1D 10 values in each row followed by the same letter are not significantly different (Analysis of covariance, P<0.05). 2Niemira and others. 2002. J Food Prot 65(9):1388–1393. 3Niemira. 2003. J Food Sci 68(9):2784–2787.

fluencing the response of pathogens to irradiation are particularly important when considering the irradiation of multicomponent foods. The overall goal is to design treatment protocols that employ the minimum efficacious dose, because excessively high doses may compromise quality, either immediately after treatment, or during storage.

Shelf-Life and Quality Changes The effects of irradiation on quality attributes of fresh-cut produce have recently been reviewed by Prakash and Foley (2004). It appears that lowdose irradiation significantly extends the shelf life of fresh-cut fruits and vegetables by inactivating spoilage microorganisms. Many fresh-cut fruits and vegetables can tolerate up to 1 kGy without significant changes in appearance or texture; some may undergo a slight softening following irradiation. Prakash and others (2000a) observed a 10% loss in firmness of Romaine lettuce at 0.35 kGy. Irradiation at 0.35 kGy had no effect on color, off-flavor, or appearance. Irradiation at 1.0 kGy, which totally eliminated L. monocytogenes and E. coli, maintained color, texture, and aroma and were preferred by taste panelists compared to other conventional treatments such as chlorination and acidification (Prakash and others 2000b). The sensory shelf life of 1.0 kGy treated celery was 29 d compared to 22 d for the control and chlorinated samples. Magee and others (2003) found that irradiation up to 1.25 kGy decreased instrumental firmness of diced Roma tomatoes. Gunes and others (2001) found irradiation at doses above 0.34 kGy reduced firmness of fresh-cut apples, while Mahrouz and others (2004) determined that 0.3 kGy enhanced the organoleptic quality of clementines. Koorapati and others (2004) showed that irradiation dose above 0.5 kGy prevented microbial-induced browning and blotches of sliced mush-

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rooms. Sections of four varieties of lettuce (red leaf, green leaf, Iceberg, and Boston) leaves taken from the midrib and leaf perimeter showed no difference in shear force when treated with doses up to 0.5kGy (Niemira and others 2002). Fan and others (2003a) showed that the shear force of Iceberg lettuce was not affected by irradiation doses up to 1 kGy, but the shear force of cilantro leaves was reduced by irradiation at 1 kGy measured on the day of irradiation (Fan and others 2003b). However, after 3, 7, or 13 d of storage at 3°C, the difference disappeared as the shear force of all samples decreased during storage. Cellular leakage (an indicator of membrane integrity) and sogginess increased in cut Iceberg lettuce (Fan and Sokorai 2002a; Fan and others 2003a) and green onions (Fan and others 2003c) when irradiated at doses above 1 kGy. Later, Fan and Sokorai (2005) measured the electrolyte leakage in 12 fresh-cut vegetables and found that the increase in electrolyte leakage was generally linear as a function of irradiation doses ranging from 0 to 3 kGy. It appears that the assessment of electrolyte leakage is an easy and fast measurement for radiation tolerance of fresh-cut fruits and vegetables. The radiation resistance was not necessarily correlated with endogenous antioxidant capacity. Irradiation at 1 kGy reduced microbial population of cut green onion leaves while maintaining or even improving sensory quality (Fan and others, 2003c). Doses higher than 1 kGy caused loss of aroma, deterioration of visual quality, and cellular leakage. Kim and others (2005) found that irradiation at doses of 0.5–1.5 kGy reduced total aerobic count and the development of decay and off-odor, improved visual quality, and preserved green color. Fan and others (2003b) found that irradiation at doses up to 2 kGy did not significantly influence overall visual quality, decay, color, texture, nutritional values, or aroma of fresh cilantro during the 14-d post-irradiation period.At a dose of 3 kGy, cilantro developed more decay, deteriorated in visual quality,and had a lower vitamin C content.Volatile compounds of fresh cilantro leaves irradiated at doses up to 3 kGy did not differ from those of controls during most of the post-irradiation period (Fan and Sokorai 2002b). Foley and others (2004) found no significant differences in yellowing, tip burn, browning, black rot, sliminess, or off-aroma among the nonirradiated cilantro leaves and those irradiated at doses up to 3.85 kGy. It appears that fresh cilantro leaves can tolerate radiation doses at least up to 2 kGy, at which most common pathogens can be completely eliminated. Respiration Rate and Headspace Atmosphere in Packages Irradiation at doses up to 2.4 kGy had little effect on the respiration rate of apple slices from four cultivars (Gunes and others 2000), but reduced

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ethylene production by the apple slices. Hagenmaier and Baker (1997) found that 0.2 and 0.5 kGy radiation increased respiration of cut Iceberg lettuce by 36% measured 1 d after irradiation; however, after 8 and 13 d storage, the irradiated samples had similar or lower respiration rates.As a result, the O2 levels in MAP packages were lower and CO2 levels were higher in irradiated samples 1–2 d after irradiation; however, after 8 or 14 d storage, the headspace concentrations were virtually the same for controls and irradiated samples. Prakash and others (2000a) found that the headspace CO2 levels in MAP of shredded cut Romaine lettuce were lower than the controls, suggesting that irradiation reduced respiration rate. The headspace atmosphere in irradiated Iceberg samples tends to have a sharper increase in CO2 and decrease in O2 (Fan and Sokorai 2002a; Fan and others 2003a), suggesting an irradiation-increased respiration. However, in the headspace of MAP of apple slices, the headspace atmosphere was similar between irradiated and nonirradiated samples (Fan and others 2005). Doses up to 0.6 kGy had little impact on the headspace gas levels of CO2 and O2 of MAP endive (Niemira and others 2004). It seems that respiration rate is generally not affected or only slightly increased temporarily by low dose radiation.Therefore, packaging materials that are currently used by the industry do not need to be altered, provided that the packaging materials are permitted by FDA. Vitamin C Vitamin C (ascorbic acid), one of the common vitamins in fresh-cut fruits and vegetables, is sensitive to irradiation. Upon irradiation, ascorbic acid in aqueous solution is easily converted to dehydroascorbic acid. However, it is important to note that dehydroascorbic acid can be regenerated back to ascorbic acid in the presence of reducing agents, and that, more generally, both ascorbic acid and dehydroascorbic acid are interconvertible and have similar biological activity.The decrease in ascorbic acid is not always observed for all fresh-cut fruits and vegetables at low doses. For example, Fan and others (2003a) did not find any difference in total ascorbic acid of Iceberg lettuce during 21 d of storage. Farkas and others (1997) found that irradiation at 1 kGy reduced ascorbic acid levels by 12% in sliced green bell pepper. During storage, the ascorbic acid content in both irradiated and nonirradiated samples decreased rapidly, particularly during an early stage (3–7 d) of storage. In the cases in which reduction of ascorbic acid by irradiation is observed, very often the decrease in ascorbic acid is relatively small compared to those variations observed among varieties and storage times. During storage, plant tissues are also capable of synthesizing ascorbic acid (Lee and Kader 2000).

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Increased Antioxidant Capacity by Irradiation Consumption of fruits and vegetables has been associated with lower incidence and lower mortality rates of cancers in human and animal systems.There is also a significant negative correlation between low intake of total fruits and vegetables and cardio- and cerebrovascular disease mortality, and high blood pressure.The protection that fruits and vegetables provide against diseases is due in part to the presence of various antioxidants, including vitamins C and E. The majority of the antioxidants in most fresh fruits and vegetables is, however, phenolic compounds. Fan (2005) studied the effect of ionizing radiation on antioxidant capacity, phenolic content, and tissue browning of three vegetables. Midrib and nonmidrib leaf tissues of Romaine and Iceberg lettuce and endive were irradiated with gamma rays at 0, 0.5, 1, and 2 kGy and then stored at 7–8°C for 8 d. Antioxidant capacity and phenolic content of tissues as well as tissue browning were analyzed at 1, 4, and 8 d of storage. In general, irradiation increased the phenolic content and antioxidant capacity of both tissue types of all vegetables at day 4 and day 8.The rates of the increase were higher in midrib tissues than in nonmidribs, and increased with storage time. Irradiation, however, increased tissue browning of midrib tissues of Romaine and Iceberg lettuce.The results suggest that irradiation increased nutritional quality of fresh-cut leafy vegetables, but some adverse visual quality changes were encountered. Because irradiation induced the synthesis of phenolic compounds, it increased the potential for tissue browning. Measures such as MAP, antibrowning agents, or other techniques may be applied in combination with irradiation to reduce the browning and softening due to irradiation. Combination of Irradiation with Other Postharvest Techniques Sanitizers Hagenmaier and Baker (1997) found that a combination of chlorination and irradiation at doses of 0.15–0.5 kGy produced fresh-cut lettuce with reduced microbial population. Lettuce irradiated at 0.81 kGy tended to have lower shear force and settled in the bag.At a dose of 0.5 kGy or less, shear force was not affected. By all measures used, the irradiated samples did spoil at roughly the same rate as did the control samples. Foley and others (2002) found that a combination of chlorination and irradiation at 5.5 kGy produced a 5.4 log reduction of E. coli O157:H7 levels in shredded Iceberg lettuce.The treatment did not cause softening of tissues, and sensory attributes were not adversely affected while it did reduce the population of microflora, mold, and yeast. Palekar and others (2004) treated whole cantaloupes with chlorine followed by low-dose electron

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beam irradiation and demonstrated that the combination treatments reduced bacterial load and extended shelf life and did not affect color, flavor, or texture of cut cantaloupe pieces, suggesting decontamination of whole cantaloupes before cutting using chlorine wash in combination with low-dose radiation may be used for shelf-life extension of sliced cantaloupe. Mahrouz and others (2004) determined that treatment with 0.3 kGy was beneficial to clementine keeping quality, if given as a single treatment.A cold water wash coupled with a waxing step caused an unacceptable increase in peel injury during storage; combining this with the 0.3 kGy treatment mitigated, but did not completely relieve, the negative impact of the washing and waxing. Hot Water Treatment Fan and others (2003a) dipped cut Iceberg lettuce in warm (47°C) water for 2 min before it was irradiated at 0, 0.5, 1, and 2 kGy radiation. Lettuce dipped at 47°C followed by irradiation at 0.5 or 1.0 kGy had better visual quality and less tissue browning than corresponding samples dipped at 5°C. Kim and others (2005) combined warm water treatment (50°C, 20 s) with low-dose radiation on fresh-cut green onions.The warm water treatment reduced the total aerobic count (TAC) by 0.9 log initially; however, in the absence of additional treatments, the microbial population regrew in storage back to the level of the control. Irradiation at all doses (0.5 to 1.5 kGy) tested in that study (Kim and others 2005) reduced TAC and the subsequent development of decay and off-odor during storage. Irradiated green onions showed improved visual quality and preserved green color.Thus, it can be concluded that irradiation at doses up to 1.5 kGy can be used to extend shelf life of fresh-cut onions. However, unlike the beneficial effects of combining irradiation with a warm-water treatment as demonstrated in lettuce (Fan and others 2003a), this combination of treatments had no clear benefits for green onions. These results highlight the difficulty in generalization across commodities when designing irradiation protocols. Mild heat treatment, applied as hot water or as a steam application, can eliminate microflora and pathogens on the surfaces of whole produce and has been suggested for potential combination treatments with irradiation (Niemira and Deschenes 2005). Freshcut fruit pieces, processed from the hot water–treated fruit, can be exposed to low dose irradiation in a sequential treatment process to further reduce or eliminate any remaining microorganisms with risk potential. Calcium and Calcium Ascorbate One major adverse effect of ionizing radiation for some fresh-cut fruits and vegetables is loss of firmness. Gunes and others (2001) found that

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a calcium dip increased firmness of sliced apples. Calcium prevented irradiation-induced softening in thin apple slices (3–4 mm thick) but was not effective with thicker wedges (Gunes and others 2001), presumably due to the lack of penetration of calcium into thick slices. Magee and others (2003) found that dipping diced Roma tomato with 1% calcium chloride or 2% calcium lactate solution enhanced firmness and decreased water-soluble pectin and increased oxalate-soluble pectin. The calcium-treated samples remained firmer than the waterdipped control. The calcium-dipped samples retained firmness; however, the flavor change due to calcium dips can be detected by some sensory panelists. Calcium ascorbate (CaA) provides not only calcium but also ascorbic acid, which is a strong antioxidant. Therefore, use of CaA can enhance firmness, reduce the negative effects of irradiation on quality, and supplement the loss in vitamin C. Fan and others (2005) treated “Gala” apple slices with water or 7% CaA followed by: (1) no further treatment, (2) irradiation at 0.5 kGy, or (3) 1.0 kGy; in that study, all samples were stored at 10°C for three weeks. Fruit slices softened during irradiation and storage, but this decrease in firmness during storage was reduced by the CaA treatment.Although the ascorbic acid content of apple slices treated with CaA decreased rapidly during storage, the ascorbic acid content was always higher in those treated samples than in the apple slices treated with water.The microflora population of apple slices was not affected by CaA, and CaA treatment did not alter the reduction in microflora by irradiation. The combination of CaA and irradiation enhanced microbial food safety while maintaining quality of fresh-cut apple slices. A point of potential concern with any chemical additive is that, in solution, antioxidants can increase radiation resistance of microorganisms by absorbing the radicals produced during the irradiation process; however, the complex chemical milieu of a food environment makes generalizations difficult (Niemira and Deschenes 2005).

Conclusion Irradiation has shown promise to improve the safety, sensory properties, and shelf-life of a wide variety of fresh and fresh-cut produce. Whether used singly or in combination with other treatments, applying irradiation in an effective, economical manner to the wide range of fruit and vegetable products in the modern food processing market presents a challenge for processors and food scientists. Varying preparation methods, storage conditions, and market forces must be considered in designing ir-

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radiation protocols that will help the fresh and fresh-cut produce industry to use this tool to provide the safest, highest-quality produce possible for consumers. References Al-Kahtani HA,Abu-Tarboush HM,Abou-Arab AA, Bajaber AS,Ahmed MA, El-Mojahadidi MA. 2000. Irradiation and storage effects on some properties of potato starch and use of thermoluminescence for identification of irradiated tubers. Amer J Potato Res 77:245–259. Auty M, Duffy G, Obeirne D, McGovern A, Gleeson E, Jordan K. 2005. In situ localization of Escherichia coli O157:H7 in food by confocal scanning laser microscopy. J Food Prot 68(3):482–486. Bari ML, Al-Haq MI, Kawasaki T, Nakauma M, Todoriki S, Kawamoto S, Isshiki K. 2004. Irradiation to kill Escherichia coli O157:H7 and Salmonella on ready-to-eat radish and mung bean sprouts. J Food Prot 67(10):2263–2268. Brescia G, Moreira R, Braby L, Castell-Perez E. 2003. Monte Carlo simulation and dose distribution of low energy electron irradiation of apple. J Food Eng 60(1):31–39. Burnett SL, Beuchat LR. 2002. Differentiation of viable and dead Escherichia coli O157:H7 cells on and in apple structures and tissues following chlorine treatment. J Food Prot 65(2):251–259. Carmichael I, Harper IS, Conventry MJ,Taylor PWJ,Wan J, Hickey MW. 1999. Bacterial colonization and biofilm development on minimally processed vegetables. J Appl Microbiol Symposium Suppl 85:45S–51S. Dewanti R, Wong ACL. 1995. Influence of culture conditions on biofilm formation by Escherichia coli O157:H7. Int J Food Microbiol 26:147–164. Diehl JF. 1995. Safety of Irradiated Foods, 2nd ed. New York: Marcel Dekker, Inc. El-Samahay SK, Youssef BM, Askar AA, Swailam HMM. 2000. Microbiological and chemical properties of irradiated mango. J Food Safety 20:139–156. Fan X, Sokorai KJB. 2002a. Sensorial and chemical quality of gamma irradiated fresh-cut iceberg lettuce in modified atmosphere packages. J Food Prot 65:1760–1765. Fan X, Sokorai KJB. 2002b. Changes in volatile compounds of gamma irradiated fresh cilantro leaves during cold storage. J Agric Food Chem 50:7622–7677. Fan X,Toivonen PMA, Rajkowski KT, Sokorai K. 2003a.Warm water treatment in combination with modified atmosphere packaging reduced undesirable effects of irradiation on the quality of fresh-cut iceberg lettuce. J Agric Food Chem 51:1231–1236. Fan X, Niemira BA, Sokorai KJB. 2003b. Sensorial, nutritional and microbiological quality of fresh cilantro leaves as influenced by ionizing irradiation and storage. Food Res Int 36:713–719. Fan X, Niemira BA, Sokorai KJB. 2003c. Use of ionizing radiation to improve sensory and microbial quality of fresh-cut green onion leaves. J Food Sci 68(4):1478–83. Fan X, Sokorai, KJB. 2005.Assessment of radiation sensitivity of fresh-cut vegetables using electrolyte leakage measurement. Postharvest Biol Technol 36:191–197. Fan X, Niemira BA, Mattheis JP, Zhuang H, Olson DW. 2005. Quality of fresh-cut apple slices as affected by low dose ionizing radiation and calcium ascorbate treatment. J Food Sci 70(2):S143–148. Fan X. 2005. Antioxidant capacity of fresh-cut vegetables exposed to ionizing radiation. J Sci Food Agric 85:995–1000.

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Farkas J, Saray T, Mohacsi-Farkas C, Horti K,Andrassy E. 1997. Effects of low dose gamma radiation on shelf-life and microbiological safety of pre-cut/prepared vegetables. Adv Food Sci 19:111–119. Fett WF. 2000. Naturally occurring biofilms on alfalfa and other types of sprouts. J Food Prot 63(5):625–632. Foley DM, Dufour A, Rodriguez L; Caporaso F, Prakash, A. 2002. Reduction of Escherichia coli O157:H7 in shredded iceberg lettuce by chlorination and gamma irradiation. Rad Phys Chem 63:391–396. Foley DM, Euper M, Caporaso F, Prakash A. 2004. Irradiation and chlorination effectively reduce Escherichia coli O157:H7 inoculated on cilantro (Coriandrum sativum) without negatively affecting quality. J Food Prot 67:2092–2098. Gorny J. 2005.A fresh look at produce safety. Food Saf Mag 11(1):70–76 Goularte L, Martins CG, Morales-Aizpurua IC, Destro MT, Franco BDGM,Vizeu DM, Huntzler BW, Landgraf M. 2004. Combination of minimal processing and irradiation to improve the microbiological safety of lettuce (Lactuca sativa L.). Rad Phys Chem 71:155–159. Guilleminot H. 1908. Comparative effects of radium and X-rays on vegetable cells. Compt Rend 145:798–801. Gunes G,Watkins CB, Hotchkiss JH. 2000. Effects of irradiation on respiration and ethylene production of apple slices. J Sci Food Agric 80(8):1169–1175. Gunes G, Hotchkiss JH, Watkins CB. 2001. Effects of gamma irradiation on the texture of minimally processed apple slices. J Food Sci 66(1):63–67. Hagenmaier RD, Baker RA. 1997. Low-dose irradiation of cut iceberg lettuce in modified atmosphere packaging. J Agric Food Chem 45:2864–2868. Hagenmaier RD, Baker RA. 1998. Microbial population of shredded carrot in modified atmosphere packaging as related to irradiation treatment. J Food Sci 63(1):162–164. Howard LR, Buescher RW. 1989. Cell wall characteristics of gamma-radiated refrigerated cucumber pickles. J Food Sci 54(5):1266–1268. Kim HJ, Hao F,Toshkov SA, Fan X. 2005 Effect of sequential treatment of warm water dip and low dose gamma irradiation and hot water wash on the quality of fresh-cut green onions. J Food Sci 70:M179-185. Koorapati A, Foley D, Pilling R, Prakash A. 2004. Electron-beam irradiation preserves the quality of white button mushroom (Agaricus bisporus) slices. J. Food Sci 69:S25–S29. Korber DR, Choi A, Wolfaardt GM, Ingham SC, Caldwell DE. 1997. Substratum topography influences susceptibility of Salmonella enteritidis biofilms to trisodium phosphate.Appl Environ Microbiol 63:3352–3358. Lafortune R, Caillet S, Lacroix M. 2005. Combined effects of coating, modified atmosphere packaging and gamma irradiation on quality maintenance of ready-to-use carrots (Daucus carota). J Food Prot 68(2):353–359. Lee SK, Kader AA. 2000. Preharvest and postharvest factors influencing vitamin C content of horticultural crops. Postharvest Biol Tech 20:207–220. Magee RL, Caporaso F, Prakash A. 2003. Effects of exogenous calcium salt treatments on inhibiting irradiation-induced softening in diced Roma tomatoes. J. Food Sci 68:2430–2435. Mahrouz M, Lacroix M, D’Aprano G, Oufedjikh H, Beoubekri C. 2004. Shelf-life and quality evaluation of clementine following a combined treatments with gamma-irradiation. Rad Phys Chem 71:141–143. Martins CG, Behrens JH, Destro MT, Franco BDGM,Vizeu DM, Hutzler B, Landgraf M. 2004. Gamma radiation in the reduction of Salmonella spp. inoculated on minimally processed watercress (Nasturtium officinalis). Rad Phys Chem 71:87–91. Maxie EC,Abdel-Kader A. 1966. Food irradiation—physiology of fruits as related to feasibility of the technology.Adv Food Res 15:105–138.

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Mercier J, Lindow SE. 2000. Role of leaf surface sugars in colonization of plants by bacterial epiphytes.Appl Environ Microbiol 66(1):369–374. Miege E, Coupe H. 1914. Influence of X-rays on plants. Compt Rend 159:338–340. Miller WR, McDonald RE, McCollum TG, Smittle BJ. 1994. Quality of ‘Climax’ blueberries after low dosage electron beam irradiation. J Food Saf 17(1):71–79. Miller WR, McDonald RE, Smittle BJ. 1995. Quality of ‘Sharpblue’ blueberries after electron beam irradiation. HortScience 30(2):306–308. Miller WR, McDonald RE. 1996. Quality of ‘Brightwell’ and ‘Tifblue’ blueberries after gamma irradiation for quarantine treatment. HortScience 31(7):1234. Monk JD, Beuchat LR, Doyle MP. 1994. Irradiation inactivation of food-borne microorganisms, J Food Prot 58(2):197–208. National Advisory Committee on Microbiological Criteria for Foods (NACMCF). 1999. Microbiological safety evaluation and recommendations on fresh produce. Food Control 10:117–134. Narvaiz P, Lescano G, Kairiyama E. 1992. Irradiation of almonds and cashew nuts. Lebensm Wiss Technol 25:232–235. Niemira BA, Sommers CH, Fan X. 2002. Suspending lettuce type influences recoverability and radiation sensitivity of Escherichia coli O157:H7. J Food Prot 65(9):1388–1393. Niemira BA. 2003. Radiation sensitivity and recoverability of Listeria monocytogenes and Salmonella on four lettuce types. J Food Sci 68(9):2784–2787. Niemira BA, Fan X, Sokorai KJB, Sommers CH. 2003. Ionizing radiation sensitivity of Listeria monocytogenes and L. innocua inoculated on endive (Cichorium endiva). J Food Prot 66:993–998. Niemira BA, Fan X, Sokorai KJB. 2004. Irradiation and modified atmosphere packaging of endive influences survival and regrowth of Listeria monocytogenes and product sensory qualities. Rad Phys Chem 72(1):41–48. Niemira BA, Deschenes L. 2005. Ionizing radiation processing of fruits and fruit products. In: Barrett DM, Somogyi L, Ramaswamy H, eds. Processing fruits: science and technology, 2nd ed. Boca Raton, FL: CRC Press, p. 221–260. Niemira BA, Solomon EB. 2005. Sensitivity of planktonic and biofilm-associated Salmonella to ionizing radiation.Appl Environ Microbiol 71(5):2732–2736. Niemira BA, Sommers CH, Ukuku D. 2005. Mechanisms of microbial spoilage of fruits and vegetables. In: Lamikanra O, Imam SH, Ukuku DO, eds. Produce degradation: reaction pathways and their prevention. (in press, CRC Press, Boca Raton, FL). Osterholm MT, Potter ME. 1997. Irradiation pasteurization of solid foods: taking food safety to the next level. Emerg Infect Dis 3(4):575–577. Palekar MP, Carbrera-Diaz E, Kalabasi-Ashtai A, Maxim JE, Miller RK, Cisneros-Zevallos L, Castillo A. 2004. Effect of electron beam irradiation on the bacterial load and sensorial quality of sliced cantaloupe. J Food Sci 69(9):M267–273. Penteado AL, Eblen BS, Miller AJ. 2004. Evidence of Salmonella internalization into fresh mangos during simulated postharvest insect disinfestation procedures. J Food Prot 67:181–184. Prakash A, Guner AR, Caporaso F, Foley DM. 2000a. Effects of low-dose gamma irradiation on the shelf life and quality characteristics of cut Romaine lettuce packaged under modified atmosphere. J Food Sci 65(3):549–553. Prakash A, Inthajak P, Huibregtse H, Caporaso F, Foley DM. 2000b. Effects of low-dose gamma irradiation and conventional treatments on shelf life and quality characteristics of diced celery. J Food Sci 65(6):1070–1075. Prakash A, Foley, D. 2004. Improving safety and extending shelf-life of fresh-cut fruits and vegetable using irradiation. In: Komolprasert V, Morehouse KM, editors. Irradiation of

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food and packaging: recent developments. Washington, D.C.: American Chemical Society, p. 90–106. Rajkowski KT, Thayer DW. 2000. Reduction of Salmonella spp. and strains of Escherichia coli O157:H7 by gamma radiation of inoculated sprouts. J Food Prot 63(7):871–875. Riordan DCR, Sapers GM,Annous BA. 2000.The survival of Escherichia coli O157:H7 in the presence of Penicillium expansum and Glomerella cingulata in wounds on apple surfaces. J Food Prot 63(12):1637–1642. Robbins JB, Fisher CW, Moltz AG, Martin SE. 2005. Elimination of Listeria monocytogenes biofilms by ozone, chlorine and hydrogen peroxide. J Food Prot 68(3):494–498. Sivapalasingam S, Friedman CR, Cohen L,Tauxe RV. 2004. Fresh produce: a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J Food Prot 67:2342–2353. Smith JS, Pillai S. 2004. Irradiation and food safety—scientific status summary. Food Tech. 58(11):48–55. Stewart PS, Mukherjee PK, Ghannoum MA. 2004. Biofilm antimicrobial resistance. In: Ghannoum MA, O’Toole GA. Microbial biofilms.Washington D.C:ASM Press, p. 250–268. Sumner SS, Peters DL. 1997. Microbiology of vegetables. In: Smith DS, Cash JN, Nip W-K, Hui YH, eds. Ch. 4. Processing vegetables: science and technology. Lancaster, PA:Technomic Publishing Inc. Takeuchi K, Frank JF. 2000. Penetration of Escherichia coli O157:H7 into lettuce tissues as affected by inoculum size and temperature and the effect of chlorine treatment on cell viability. J Food Prot 63(4):434–440. Thayer DW, Rajkowski KT. 1999. Developments in irradiation of fresh fruits and vegetables. Food Technol 53(11):62–65. World Health Organization (WHO). 1999. High-dose irradiation: wholesomeness of food irradiated with doses above 10 kGy. Joint FAO/IAEA/WHO Study Group on High-Dose Irradiation, Geneva, 15–20 September 1997, in WHO Technical Report Series 890, 1999. Yu L, Reitmeier CA, Love MH. 1996. Strawberry texture and pectin content as affected by electron beam irradiation. J Food Sci 61(4):844–846.

Disclaimer Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 11 IRRADIATION OF SEAFOOD WITH A PARTICULAR EMPHASIS ON LISTERIA MONOCYTOGENES IN READY-TO-EAT PRODUCTS Denise M. Foley, Ph.D.

Introduction In the period between 1993 and 1997, foodborne disease outbreaks implicating seafood were five times more frequent than those linked to beef, 19 times more than pork, four and 12 times those of chicken and turkey, respectively (Olsen and others 2000). When the etiologic agent was identified, the implicated organisms included Hepatitis A and Norwalk viruses as well as Salmonella, Shigella, C. perfringens, and Vibrio parahaemolyticus (Olsen and others 2000).

Listeria monocytogenes Is a Significant Contaminant of Seafood Although the International Commission on Microbiological Specifications for Foods (ICMSF) recommends an acceptable level of f100 L. monocytogenes per g in certain foods for healthy individuals (ICMSF 1994), in 1986, the FDA and USDA established a zero-tolerance policy for L. monocytogenes in ready-to-eat (RTE) foods. If samples test positive for L. monocytogenes, the product is adulterated. Current U.S. regulations, effective in October of 2003, stipulate that establishments that produce RTE meat and poultry products that support the growth of L. monocytogenes and are exposed to the environment after lethal treatments must 185

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have in their Hazard Analysis Critical Control Point (HACCP) plans sanitation standard operating procedures, or other prerequisite programs or controls that prevent adulteration with L. monocytogenes (FSIS 2003). Although outbreaks attributed to L. monocytogenes in seafood have been infrequent (Ericsson and others 1997; Miettinen and others 1999), seafood salad and smoked fish both have been demonstrated to be the types of RTE products most often contaminated with this pathogen. Its presence has caused numerous recalls and has been responsible for considerable economic losses. During the years 2000–2002, the FDA issued 37 Class I recalls of seafood due to contamination with L. monocytogenes (FDA 2003). In addition, during the period between Jan 2000 and Nov 2001, when more than 31,000 ready-to-eat products were tested for the presence of L. monocytogenes, 4.7% of the seafood salad samples (of 2,446 samples) and 4.31% of the smoked seafood (of 2,644 samples) tested positive.These were the highest prevalence rates for the product categories in the study (Gombas 2003).When investigating a smaller sample size, Hartemink and Georgsson (1991) found that 16% of seafood salads in the Icelandic market tested positive for the presence of L. monocytogenes and in Belgium, 27% of seafood salads tested positive (Uyttendaele, 1999). Additionally, Lack and others (1996) reported that 30% of RTE salads in Germany were contaminated with L. monocytogenes and, in particular, those containing highly perishable ingredients, such as surimi, constituted a health risk. For smoked fish, in Sweden, 10.7% of various samples harbored L. monocytogenes, 10 (of 150) of the samples at levels greater than 100 cfu/g (Loncarevic and others 1996) but Jemmi (1990) reported that 25% of tested samples of smoked salmon in Switzerland were contaminated. Clearly, these products are at risk for initiating a foodborne illness. Cold smoking has little effect on the pathogen (Jahncke and others 2004); furthermore, L. monocytogenes can multiply in smoked fish, as clearly demonstrated by Guyer and Jemmi (1991). Interestingly, BenEmbarek (1994) indicated in his review article that the overall prevalence of Listeria ssp. in smoked fish products (hot and cold process) was comparable, 9 and 10%, respectively, despite the fact that Listeria could not survive the hot smoke process. The author indicated that although a clear route of contamination for the products was not identified, post-processing contamination was likely to blame. Furthermore, given the widespread distribution of the organism, it is not surprising that several studies have concluded that the processing plant environment is the major source of L. monocytogenes contamination for smoked seafood and other RTE products (Hicks and others 2004, and references within).

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Stress Adaptation of the Organism Seafood salad safety is based on the hurdle concept. It combines the hurdles of refrigerated storage, the use of preservatives, and the addition of organic acids to lower the pH.These steps are considered “hurdles”to the foodborne pathogen and together they additively provide food safety. However, if the organism is stress adapted, it may counteract the effectiveness of the food preservation hurdles and compromise food safety (Lou and Yousef 1997). Various food poisoning microorganisms can become more resistant to lethal processes after exposure to sublethal stress factors such as starvation, heat, and low pH.This phenomenon is referred to as stress adaptation (Yousef and Courtney 2003). L. monocytogenes exhibits stress adaptation through an evolved stress response system.The system appears to induce protective responses that allow the organism to better tolerate severe acid, thermal and osmotic stress, crystal violet, ethanol, high carbon dioxide atmospheres, bacteriocins, and hydrogen peroxide (O’Driscoll and others 1996; Francis and O’Beirne 2001; Lou and Yousef 1997; Jørgenson and others 1995). It has been noted that survival in a normally lethal pH 3.5 is enhanced by at least 1,000-fold after acid adaptation (Hill and Gahan 2000). One obvious question that has lately been under investigation is whether the stress response system will allow L. monocytogenes to become more resistant to irradiation.

Irradiation Is an Effective Post-Processing Treatment for Fish Products Scientific studies conducted worldwide over the past 40 years have shown the benefits of radiation processing for the preservation and microbial quality improvement of fish and seafood. These studies are reviewed in the paper by Venugopal and others (1999) and in the book chapter by Andrews and Grodner (2004).Although it is known that lowfat fish tolerate higher doses of irradiation, Kamat and Thomas (1999) investigated whether the fat content of irradiated fish influenced survival and post-irradiation recovery of bacterial pathogens.They found that the fat content and, presumably, the products of lipid peroxidation did not appear to affect the lethality of irradiation treatment and, furthermore, recovery and growth were not influenced by fat levels. In another recent study, Savvaidis and others (2002) investigated the effect of irradiation on vacuum-packaged fresh trout. The authors demonstrated that a 2 kGy dose followed by refrigeration at 4°C would extend the shelf life of the

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product from seven to 28 days.Various naturally occurring microbial populations were reduced but, more important, this dose resulted in a 2 log reduction of inoculated L. monocytogenes after 18 days of storage. Although the authors of that study did not report the reduction of L. monocytogenes that occurred immediately after irradiation, Kamat and Thomas (1999) reported a D10 value of L. monocytogenes strain 0136 in 10% fish homogenates as 0.2–0.3 kGy based on the exponential portion of the curve, but a tailing effect was noted. L. monocytogenes has been often reported to possess a D10 value of between 0.30 and 0.45 kGy (Jay 2002; Huhtanen and others 1989). The D value for L. monocytogenes is similar to that of Staphylococcus aureus (0.34 kGy) in surimi (Jaczynski and Park 2004) and shrimp (0.29 kGy) products (Venugopal and others 1999) (Table 11.1). While investigating the effects of common additives in combination with irradiation, Jeevanandam and others (2001) found that fresh threadfin bream salted and irradiated at 1 or 2 kGy demonstrated a shelf life of 14 and 28 days, respectively, compared to nine days for salting alone. Salting did not have a significant effect on shelf life but did result in reduced drip formation and enhanced texture. In good agreement with these findings, Chouliara and others (2004) concluded that vacuumTable 11.1. D10 Values of the Common Pathogenic Contaminants Listeria monocytogenes and Staphylococcus aureus in Various Food Matrices Food System

D-value (kGy)

Shrimp, mackerel, golden anchovy 0–2 °C Surimi seafood salad

0.15–0.25

0.23–0.3

Crabmeat

0.59 ± 0.02

10% Fish homogenate Mashed potatoes

0.2–0.3

Mashed potatoes Roast beef Salisbury steak

0.53 ± 0.05 0.50 ± 0.07 0.43* 0.64 ± .061 .40 ± .054 0.85*

Strain

Reference

(Venugopal, Doke, and Thomas 1999) L. monocytogenes (Foley and others (16397, 1992, 0733) 2005) acid adapted L. monocytogenes (Chen,Andrews, naturally occurring and Grodner 1996) L. monocytogenes (Kamat and 0136 Thomas 1999) L. monocytogenes (Grant and P(10)4, CRA711 Patterson 1992) L. monocytogenes (Clardy and others (16397, 0733, 1992) 2002) L. monocytogenes (Grant and P(10)4, CRA711 Patterson 1992) L. monocytogenes (Clardy and others (16397, 0733, 1992) 2002) L. monocytogenes

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Table 11.1. D10 Values of the Common Pathogenic Contaminants Listeria monocytogenes and Staphylococcus aureus in Various Food Matrices (continued) Food System

D-value (kGy)

Frankfurters, bologna, ham, and roast beef

0.42–0.44

Ground pork

0.66

Beef, lamb, pork, turkey breast, turkey legs Ham-cheese sandwich ⫺40°C Mozzarella cheese ⫺40°C Deli turkey

0.45–0.50

Cheese-tortilla interface Deli turkey-tortilla interface Cheese-turkey interface Surimi

0.71–0.81 1.4 0.58; 0.65

Strain L. monocytogenes (Scott A, H7764, H7969, H7962, OB90393) L.monocytogenes Scott A- starved L. monocytogenes (15313, 43256, 49594, 7644) L. monocytogenes Presque Isle cultures L.monocytogenes Scott A L. monocytogenes (H7762, H7764, F4249, F4561)

(Foong and others 2004)

S. aureus (138-cps,146-cps, 153-cps,648-gf, 649-gf, 657-gf) S. aureus

(Jaczynski and Park 2004)

0.25; 0.33 0.33; 0.41 0.34

0.29 0.16 ± 0.02

S. aureus naturally occurring

Ham-cheese sandwich ⫺40°C Ground beef 0°C and ⫺20°C

0.62–0.63

S. aureus ATCC 8095

*estimated

(Mendonca and others 2004) (Thayer and Boyd 1995,Thayer and others 1995) (Foley and others 2001) (Hashisaka and others 1989) (Sommers and Boyd 2005)

0.27; 0.37

Prawns ⫺10°C Crabmeat

Deboned chicken meat 0°C Bison, ostrich, alligator, caiman meat

Reference

0.51 ± 0.02, 0.88 ± 0.05 0.36 0.37 ± 0.0

S. aureus (B124,ATCC#s 25923,13565, 14458, 27154) S. aureus ATCC 13565 S. aureus (ATCC 13565, ATCC 25923, B124)

(Venugopal, Doke, and Thomas 1999) (Chen,Andrews, and Grodner 1996) (Lamb and others 2002) (Thayer and Boyd 2001)

(Thayer and Boyd 1992) (Thayer and others 1997)

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packaged, salted sea bream (Sparus aurata) irradiated at either 1 or 3 kGy had a shelf life of 27–28 days compared to the nonirradiated controls, which lasted 14–15 days.The shelf life extension was based on fivemember panel sensory evaluation. Additionally, irradiation at 2.5 kGy effectively controlled the microbial population during 12 weeks of refrigerated storage of a low-salt recipe of aged seasoned intestine of Alaska Pollack (Theragra chalcogramma) (Jo and others 2004).This traditional Korean fermented dish is called Changran Jeotkal, and the irradiated, lower salt recipe was found to have immediate application for the industry as no adverse effect on sensory qualities was noted by a 50-member consumer panel. Similarly, various preservatives have been tested in combination with low-dose irradiation with resultant benefits on Dover sole, whale meat, and horse mackerel.These formulations have included 0.1% sodium benzoate, potassium sorbate, sodium salts of methyl and propyl esters of parahydroxybenzoic acid, or 0.002% of furyl furamide (Shiflett 1965; Tomiyama and others 1969). In addition, Bari and others (2000) found that combinations of ascorbic acid additive and 5 kGy irradiation would extend the shelf life of commercially prepared fried fish cutlet in Bangladesh (stored at room temperature) by 14 days. Preparing the fish under more sanitary laboratory conditions could extend the shelf life to five weeks. The previously mentioned finding underscores the need to use irradiation in combination with good manufacturing practices (GMPs) for maximum benefit and safety.The finding is also in agreement with earlier work by Laycock and Regier (1970), who demonstrated that significant extensions of the shelf life of irradiated haddock fillets occurred even for fish of low initial quality (older). However, the older fish were said to be borderline in acceptance for most of the extended storage life period, whereas fish of higher initial quality prior to irradiation were judged to be borderline only in the later part of the extended study. The studies described briefly here and others conducted over the last several decades indicate that irradiation can be a useful tool in increasing the shelf life and safety of seafood products. However, if ionizing radiation is to be used as a preservation factor and hurdle in the food industry, it is important to understand whether an organism can become resistant to this treatment. Although studies such as those conducted by Huhtanen and others (1989) show that L. monocytogenes isolated from irradiated product do not show an increase in radiation resistance, we did observe a consistent trend of increased radiation resistance after one hour of exposure to Tryptic Soy Broth brought to pH 5.5 with acetic acid, citric acid, or lactic acid (Foley and others 2005).The trend was repeatable but not significant (p=0.054).The increased resistance did not occur if cells

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were exposed for four hours prior to radiation. Surprisingly, the increased resistance did not occur when the acid-exposed cells were placed in a surimi-based seafood salad (pH 5.1) and irradiated. In this case, the cells were more sensitive to irradiation than the cells not exposed to acid prior to introduction into the seafood salad. When testing acid-adapted organisms, it appears that the acidic seafood salad environment acts as a hurdle in combination with the irradiation despite acid-adaptation of L. monocytogenes (Foley and others 2005).This is in agreement with data from Sommers and others (2003) in which L. monocytogenes inoculated onto frankfurters dipped in citric acid (pH<4.0) showed increased radiation sensitivity and inhibited the growth of radiation-damaged L. monocytogenes during long-term refrigerated storage. Similar increases in radiation sensitivity were also observed in RTE meats that incorporated sodium diacetate and potassium lactate mixtures (Sommers and Fan 2003; Sommers and others 2003). In the case of surimi, the combination of exposure to acetic acid acidified Tryptic Soy Broth prior to introduction into seafood salad that was subsequently irradiated acted as cumulative stressors. Instead of increasing resistance to irradiation, acid exposure prior to introduction into the salad increased the sensitivity. Perhaps even more interesting is the finding by Mendonca and others (2004) that starvation of exponential phase cells in 0.85% NaCl for eight days at 25°C was the best at inducing a protective response in irradiated saline and ground pork.The D10 values for starved cells in saline and pork were 0.21 and 0.66 kGy, respectively, compared to 0.07 and 0.35 kGy for the controls. Furthermore, these authors found that stationary cells had an intermediate D10 value of 0.09 and 0.42 kGy in saline and pork, respectively. Despite the slight decrease in the effectiveness of radiation sometimes induced by the stress response system, it is important to note that although significant, the difference is not the 1,000-fold greater resistance reported for extreme acid tolerance (Hill and Gahan 2000).

Physical, Chemical, and Sensory Changes of Irradiated Seafood Irradiation can cause undesirable organoleptic changes in products.The dose administered, subsequent processing, and components within the product will determine the threshold dose of the product, after which undesirable changes occur. In general, doses of 1–2 kGy are well tolerated by lightly pigmented seafoods (Andrews and Grodner 2004). Irradiation may cause bleaching of salmon fillets, possibly due to bleaching of the pigment asthaxanthin (Licciardello and Ronsivalli 1982;

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Hultmann and Rustad 2004). However, Jaczynski and Park (2004) noted that doses of 1 and 2 kGy resulted in significantly whiter surimi seafood crabsticks, a characteristic associated with higher quality. Four kGy did not improve the whiteness over what was already observed at 2kGy, and sample temperature as well as the presence or absence of oxygen did not affect the color. The lipid content of fish does impact the usefulness of irradiation processing. Lean fish species are known to undergo the least amount of irradiation-induced rancidity (Venugopal and others 1999). For example, the lipid content of Spanish mackerel (Scombermorus maculatus) is 6.30g/100g and, thus, it is considered a medium-fat-content fish.This can be compared to 0.6–1.08g lipid/100g for crab, a low-fat-content product (Silva and Chamul 2000). In a study employing Indian mackerel, a fish also described as “medium” in its fat content, a shelf life of 25–30d was achieved without undergoing any rancid changes when irradiated at 1.5 kGy, compared to the control, which lasted 10–12 days (Venugopal and Nair 1992).Additionally,Andrews and Grodner (2004) reviewed the optimum doses tolerated by several seafood products.The optimum dose was the dose that provided the longest shelf life without negatively impacting sensory qualities. In general, doses of 1–2 kGy were well tolerated with some species of molluscan shellfish displaying optimum doses of up to 4.5 Gy. Interestingly,Andrews and Grodner (1994) noted that, in crayfish tails, the acceptability of texture and juiciness was markedly reduced as the irradiation dose exceeded 2 kGy.The authors noted that the dose necessary for an acceptable reduction of L. monocytogenes (4 logs) was very close to the threshold dose for the product, a point that must be considered carefully for any product being considered for irradiation processing. Of further interest is the fact that despite the high oil and fat content of mayonnaise, we did not observe a significant organoleptic change in the 0.7 kGy–irradiated surimi-based seafood salad as determined by consumer panel.This dose was sufficient to achieve at least a 3 log reduction in inoculated L. monocytogenes (Foley and others 2005).

Competing Microflora A frequent question regarding irradiation processing asks what effect the elimination or reduction of a microbial flora has on the inhibition of pathogen multiplication. In our previous study, populations of L. monocytogenes did not grow in the seafood salad, despite the absence of competition in the 4.5 kGy irradiated samples (Foley and others 2005). Perhaps the presence of preservatives in the salad inhibited Listeria multiplica-

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tion, because we did not see multiplication in this particular salad under any tested storage condition. The preservatives (sodium benzoate and potassium sorbate) did not appear to inhibit the observed populations of yeast and mold. However, in the study by Savvaidis and others (2002), L. monocytogenes grew in vacuum-packaged trout in the presence of background flora.Additionally, the lack of effect of the presence or absence of background flora on the rate of multiplication of L. monocytogenes in a food has been described previously. Grant and others (1993) reported that the growth rates of L. monocytogenes in irradiated and nonirradiated roast-beef and gravy were similar, but survivors of the radiation processing experienced an extended lag. Reduced levels of background flora did not seem to enable faster replication. More convincing is the study by Barakat and Harris (1999), who reported that the presence or absence of a competing lactic acid and Bronchothrix containing microbiota did not affect the rate of growth of L. monocytogenes or Yersinia enterocolitica in modified atmosphere packaged poultry product. In their study, sodium lactate and ALTA 2341 preservatives added at the maximum recommended levels also extended the lag phase of the pathogens, but storage temperature was the most important growth-inhibiting factor.

Comments Regarding Irradiation and the Risk for Botulism Some have voiced a concern relating to the potential for Clostridium botulinum outgrowth and toxin production (especially strain types B, E, and F, which grow at temperatures as low as 3.3°C) after irradiation processing. It is known that spore-forming organisms are much more resistant to irradiation and would not be destroyed at the doses described within this article. However, it occurs to us that packaging methods (that do not exclude oxygen) as well as temperature of storage (3°C or less) will be key to future investigations of safety. In fact, Shewan and Hobbs (1970), in reference to C. botulinum types E, F, and non-proteolytic type B, concluded,“. . .in particular if the temperature of the produce is never allowed to exceed 3°C, there should be no danger from botulinum poisoning, even if irradiation is employed.” Additionally, Licciardiello and Ronsivalli (1982) have stated that “low dose irradiation of fish would present no botulism hazard if the product were maintained at a storage temperature below 41–42°F (5–5.5°C).” Furthermore, they point out that “low-dose irradiation is not unique in its ability to alter the microflora. Other currently accepted processes such as thermal pasteurization of crabmeat have the same effect and, although a similar botulism hazard may be associated with such treatments, none has occurred in the many

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years of usage.” In addition to strict temperature control, the use of nitrite, in smoked fish, would add another protection in preventing the outgrowth of spores and toxin production. Conclusion Because contamination of RTE seafood with L. monocytogenes and other pathogens is a concern, there is a critical need to evaluate postprocessing interventions to reduce or eliminate the threat.There is a particular desire to implement processes that can be administered post packaging. Irradiation is an effective process that can be administered post packaging and holds promise for improving the safety of seafood products. References Andrews LS, Grodner RM. 1994. Gamma irradiation of Listeria monocytogenes in crayfish. In: Proceedings of the 17th annual conference, tropical and subtropical fisheries society of America 17:118–122. Andrews LS, Grodner RM. 2004. Ionizing Radiation of Seafood. In: Komolprasert V, Morehouse KM, eds. Irradiation of Food and Packaging: Recent Developments.Washington, D.C.:American Chemical Society, p. 151–164. Barakat RK, Harris LJ. 1999. Growth of Listeria monocytogenes and Yersinia enterocolitica on cooked modified-atmosphere-packaged poultry in the presence and absence of a naturally occurring microbiota.Appl Environ Microbiol 65(1):342–345. Bari ML, Sabina Y, Kusunoki H, Uemura T. 2000. Preservation of fish cutlet (Pangasius pangasius) at ambient temperature by irradiation. J Food Prot 63(1):56–62. Ben-Embarek PK. 1994. Presence, detection and growth of Listeria monocytogenes in seafoods: a review. Int J Food Microbiol 23(1):17–34. Brett MSY, Short P, McLauchlin J. 1998. A small outbreak of listeriosis associated with smoked mussels. Int J Food Microbiol 43(3):223–229. Chen YP,Andrews LS, Grodner RM. 1996. Sensory and microbial quality of irradiated crab meat products. J Food Sci 61(6):1239–1242. Chouliara I, Savvaidis IN, Panagiotakis N, Kontominas MG. 2004. Preservation of salted, vacuum-packaged, refrigerated sea bream (Sparus aurata) fillets by irradiation: microbiological, chemical and sensory attributes. Food Microbiol 21:351–359. Clardy S, Foley DM, Caporaso F, Calicchia ML, Prakash A. 2002. Effect of gamma irradiation on Listeria monocytogenes in frozen, artificially contaminated sandwiches. J Food Prot 65(11):1740–1744. Ericsson H, Eklow A, Danielsson-Tham ML, Loncarevic S, Mentzing LO, Persson I, Unnerstad H,Tham W. 1997.An outbreak of listeriosis suspected to have been caused by rainbow trout. J Clin Microbiol 35:2904–2907. FDA. 2003. Recalls and field corrections. Available at: http://www.fda.gov/bbs/topics/enforce/ENF00628.html.Accessed on:August 20, 2003.

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Foley DM, Reher E, Caporaso F, Trimboli S, Musherraf Z, Prakash A. 2001. Elimination of Listeria monocytogenes and changes in physical and sensory qualities of a prepared meal following gamma irradiation. Food Microbiol 18(2):193–204. Foley DM, Trimboli SL, Lamb J, Gogley J, Thompson J, Caporaso F, Calicchia M, Prakash A. 2005.Acid-adaptation does not increase the resistance of Listeria monocytogenes to irradiation in a seafood salad. Int J Food Microbiol 99:147–156. Foong SCC, Gonzalez GL, Dickson JS. 2004. Reduction and survival of Listeria monocytogenes in ready-to-eat meats after irradiation. J Food Prot 67:77–82. Francis GA, O’Beirne D. 2001. Effects of acid adaptation on the survival of Listeria monocytogenes on modified atmosphere packaged vegetables. Int J Food Sci Technol 36(5):477–487. [FSIS] Food Safety and Inspection Services. 2003. 9CFR part 430 Control of Listeria monocytogenes in Ready-to-eat meat and poultry products; Final rule. Available at: http:// www.fsis.usda.gov/OPPDE/rdad/FRPubs/97-013F.pdf.Accessed on: March 30, 2005. Gombas DE, Chen Y, Clavero RS, Scott VN. 2003. Survey of Listeria monocytogenes in Ready-to-Eat Foods. J Food Prot 66(4):559–569. Grant LR, Nixon CR, Patterson MF. 1993. Comparison of the growth of Listeria monocytogenes in unnirradiated and irradiated cook-chill roast beef and gravy at refrigeration temperatures. Lettr.Appl. Microbiol. 17: 55-57. Grant IR, Patterson MF. 1992. Sensitivity of foodborne pathogens to irradiation in the components of a chilled ready meal. Food Microbiol 9(2):95–103. Guyer S, Jemmi T. 1991. Behavior of Listeria monocytogenes during fabrication and storage of experimentally contaminated smoked salmon. Appl Environ Microbiol 57(5): 1523–1527. Hartemink R, Georgsson F. 1991. Incidence of Listeria species in seafood and seafood salads. Int J Food Microbiol 12(2/3):189–195. Hashisaka AE,Weagant SD, Dong FM. 1989 Survival of Listeria monocytogenes in mozzarella cheese and ice cream exposed to gamma irradiation. J Food Prot 52: 490-492. Hicks D,Wiedmann M, Scott VN, Collette R, Jahncke ML, Gall K. 2004. Minimizing Listeria contamination in smoked Seafood: Training Plant Personnel. J Food Prot Trends 24:953–960. Hill C, Gahan C. 2000. Listeria monocytogenes: role of stress in virulence and survival in food. Irish J Agri Food Res 39(2):195–201. Huhtanen CN, Jenkins RK,Thayer DW. 1989. Gamma radiation sensitivity of Listeria monocytogenes. J Food Prot 52(9):610–613. Hultmann L, Rustad T. 2004. Iced storage of Atlantic salmon (Salmo salar)—effects on endogenous enzymes and their impact on muscle proteins and texture. Food Chem 87(1): 31–41. [ICMSF] International Commission on Microbiological Specifications for Foods. 1994. Choice of sampling plan and criteria for Listeria monocytogenes. Int J Food Microbiol 22(2-3):89–96. Jaczynski J, Park JW. 2004.Application of electron beam to surimi seafood. In: Komolprasert V, Morehouse KM, eds. Irradiation of Food and Packaging: Recent Developments. Washington, D.C.:American Chemical Society, p. 165–179. Jahncke ML, Collette R, Hicks D,Weidmann M, Scott VN, Gall K. 2004.Treatment options to eliminate or control growth of L. monocytogenes on raw material and on finished product for the smoked fish industry. Food Prot Trend 24(8):612–619. Jay J. 2002. Modern Food Microbiology, 6th ed. Gaithersburg, Maryland: Aspen Publishers Inc.

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Jeevanandam K, Kakatkar A, Doke SN, Bongirwar DR,Venugopal V. 2001. Influence of salting and gamma irradiation on the shelf-life extension of threadfin bream in ice. Food Res Int 34(8):739–746. Jemmi T. 1990. Actual knowledge of Listeria in meat and fish products. Mitt Geb Lebensmittelunters Hyg 81:144–157. Jo C, Lee WD, Kim DH, Kim JH, Ahn HJ, Byun MW. 2004. Quality attributes of low salt Changran Jeotkal (aged and seasoned intestine of Alaska pollock, Theragra chalcogramma) developed using gamma irradiation. Food Control 15(6):435–440. Jørgensen F, Stephens PJ, Knøochel S. 1995. The effect of osmotic shock and subsequent adaptation on the thermotolerance and cell morphology of Listeria monocytogenes. J Appl Bacteriol 79:274–281. Kamat A,Thomas P. 1999. Recovery and growth of some food-borne pathogens in irradiated low and high fat fish during storage at 2–4C. J Food Safety 19(1):35–44. Lack WK, Becker B, Holzapfel WH. 1996. Hygenic quality of pre-packed ready-to-serve salads in 1995.Archiv für Lebensmittelhygiene 47(6):129–152. Lamb JL, Gogley JM,Thompson MJ, Solis DR, Sen S. 2002. Effect of low-dose gamma irradiation on Staphylococcus aureus and product packaging in ready-to-eat ham and cheese sandwiches. J Food Prot 65(11):1800–1805. Laycock A, Regier LW. 1970.The effect of gamma irradiation on the microbial spoilage patterns on fish, in relation to initial quality. In: Preservation of Fish by Irradiation: proceedings of a panel on the irradiation preservation of foods of marine origin/organized by the joint FAO/IAEA Division of Atomic Energy in Food and Agriculture. Vienna: International Atomic Energy Agency, p. 13–26. Licciardiello JL, Ronsivalli LJ. 1982. Irradiation of Seafood. In: Martin RE, Flick GJ, Hebard CE,Ward D, eds. Chemistry and Biochemistry of Marine Food Products.Westport, Connecticut:AVI Publishing Co., p. 305–322. Loncarevic S, Tham W, Danielsson-Tham ML. 1996. Prevalence of Listeria monocytogenes and other Listeria ssp. in Smoked and “Gravad” fish.Acta Vet Scand 37:13–18. Lou Y, Yousef AE. 1997. Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. App Env Microbiol 63(4): 1252–1255. Mendonca AF, Romero MG, Lihono MA, Nannapaneni R, Johnson MG. 2004. Radiation resistance and virulence of Listeria monocytogenes Scott A following starvation in physiological saline. J Food Prot 67(3):470–474. Miettinen MK, Siitonen A, Heiskanen P, Haajanen H, Bjorkroth KJ, Korkeala HJ. 1999. Molecular epidemiology of an outbreak of febrile gastroenteritis caused by Listeria monocytogenes in cold-smoked rainbow trout. J Clin Microbiol 37(7):2358–2360. O’Driscoll B, Gahan CGM, Hill C. 1996.Adaptive acid tolerance response in Listeria monocytogenes: isolation of an acid-tolerant mutant which demonstrates increased virulence.App Env Microbiol 62(5):1693–1698. Olsen SJ, MacKinon LC, Goulding JS, Bean NH, Slutsker L. 2000. Surveillance for foodborne disease outbreak, United States, 1993–1997. Morbidity Mortality Weekly Report. 49(SS01):1–51. Available at: http://www.cdc.gov/epo/mmwr/preview/mmwrhtml/ ss4901a1.htm.Accessed on:April 14, 2005. Savvaidis IN, Skandamis P, Riganakos KA, Panagiotakis N, Kontominas MG. 2002. Control of natural microbial flora and Listeria monocytogenes in vacuum-packaged trout at 4 and 10 degrees C using irradiation. J Food Prot 65(3):515–522. Shewan JM, Hobbs G. 1970.The botulism hazard in the proposed use of irradiation of fish and fishery products in the United Kingdom. In: Preservation of Fish by Irradiation. Vienna: International Atomic Energy Agency, p. 123.

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Shiflett MA. 1965. Preservation of Dover sole by low-dose irradiation and antimicrobial agents. In: Martin RE, Flick GJ, Hebard CE,Ward D, eds. Chemistry and Biochemistry of Marine Food Products.Westport, Connecticut:AVI Publishing Co., p. 1982. Silva JL, Chamul RS. 2000. Composition of Marine and Freshwater finfish and shellfish species and their products. In: Martin R, Carter EP, Flick G, Davis LM, eds. Marine and Freshwater Products Handbook. Lancaster, Pennsylvania: Technomic Pub Co Inc., p. 31–46. Sommers CH, Boyd G. 2005. Elimination of Listeria monocytogenes from Ready-to-Eat Turkey and Cheese Tortilla Wraps Using Ionizing Radiation. J Food Prot 68(1):164–167. Sommers CH, Fan X. 2003. Gamma Irradiation of Fine-Emulsion Sausage Containing Sodium Diacetate. J Food Prot 66(5):819–824. Sommers CH, Fan X, Niemira BA, Sokorai K. 2003. Radiation (Gamma) Resistance and Postirradiation Growth of Listeria monocytogenes Suspended in Beef Bologna Containing Sodium Diacetate and Potassium Lactate. J Food Prot 66(11):2051–2056. Thayer DW, Boyd G. 1992. Gamma ray processing to destroy Staphylococcus aureus in mechanically deboned chicken meat. J Food Sci 57(4):848–851. Thayer DW, Boyd G. 1995. Radiation sensitivity of Listeria monocytogenes on beef as affected by temperature. J Food Sci 60(2):237–240. Thayer DW, Boyd G. 2001. Effect of irradiation temperature on inactivation of Escherichia coli O157:H7 and Staphylococcus aureus. J Food Prot 64(10):1624–1626. Thayer DW, Boyd G, Fox JB, Jr., Lakritz L. 1997. Elimination by gamma irradiation of Salmonella spp. and strains of Staphylococcus aureus inoculated in bison, ostrich, alligator, and caiman meat. J Food Prot 60(7):756–760. Thayer DW, Boyd G, Fox Jr. JB, Lakritz L, Hampson JW. 1995.Variations in radiation sensitivity of foodborne pathogens associated with the suspending meat. J Food Sci 60(1): 63–67. Tomiyama T, Jeng SS, Shiraishi E, Hamada M,Yamada Y. 1969. Complementary effect of food preservative and gamma irradiation of whale and horse mackerel flesh. In: Kreuzer R, ed. Freezing and Irradiation of Fish. London: Fishing News (Books) Ltd., p. 472–477. Uyttendaele M,Troy Pd, Debevere J. 1999. Incidence of Listeria monocytogenes in different types of meat products on the Belgian retail market. Int J Food Microbiol 53(1):75–80. van Schaik W, Gahan CGM, Hill C. 1999.Acid-adapted Listeria monocytogenes displays enhanced tolerance against the lantibiotics nisin and lacticin 3147. J Food Prot 62(5): 536–539. Venugopal V, Doke SN,Thomas P. 1999. Radiation processing to improve the quality of fishery products. Crit Rev Food Sci Nutr 39(5):391–440. Venugopal V, Nair PM. 1992. Radiation preservation of seafoods: A case study on Indian mackerel. Fishery Technol (India) 29:114–123. Yousef AE, Courtney PD. 2003. Basics of stress adaptation and implications in newgeneration foods. In:Williams JA, Juneja VK,Yousef AE, eds. Microbial Stress Adaptation and Food Safety. Boca Raton, Florida: CRC Press, p. 2.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 12 IONIZING RADIATION OF EGGS I. Álvarez, B.A. Niemira, X. Fan, and C.H. Sommers

Introduction The chicken egg, as a stand-alone product or as a food ingredient, is a nutritious part of the Western diet and an important component of a wide variety of foods due to the functional properties of the yolk and white (foaming, emulsifying, gelling). However, eggs are responsible for an estimated 230,000 cases of foodborne illnesses each year, resulting in economic losses and representing a consistent and serious obstacle to the well-being of consumers (Bufano 2000). Eggs can be externally (horizontal transmission) or internally (vertical or transovarian transmission) contaminated by different microorganisms, among which Salmonella is the most significant, particularly Salmonella serovar Enteritidis, which is the leading cause of all egg-related foodborne illnesses (Anonymous 2002). To reduce and ultimately eliminate Salmonella-related illnesses in eggs and egg products, two basic agronomic strategies have been followed. The first is to maintain rigorous on-farm agricultural and sanitation practices that include the vaccination of hens against Salmonella.With these practices, the Salmonella-presence in shell-eggs could be reduced, but eradication remains very difficult.The second strategy is the application of processes to destroy pathogens in egg and egg products at the processor level.Washing with antimicrobial solutions, heat, and UV irradiation of eggs have been used to destroy external pathogenic contamination of shell-eggs. Nevertheless, none of these techniques is effective against internal contamination of Salmonella, since the bacteria are sheltered from their lethal effect by the egg shell. For egg products, heat pasteurization has been employed as a hygienization system. However, current heat pasteurization treatments (for example, for liquid whole egg 60°C/3.5 min in the 199

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United States, 64.4° C/2.5 min in the UK, or 70°C/1.5 min—ultrapasteurization) could not assure the safety and security of egg products contaminated with isolates possessing very high heat resistance, such as Salmonella serovar Senftenberg 775W (D60°C=3 min, z=5.2°C). More intensive heat treatments targeting these types of isolates cause deteriorated quality and would therefore not allow producers to offer a product with nutritional and functional properties similar to those of the untreated, fresh product (Mañas and others 2003).Therefore, it is necessary to identify a technology that provides for the destruction of pathogenic contamination of shell-eggs and egg products with a minimum impact on their freshness properties. Ionizing radiation (IR) is a means of food preservation that has been in development since the early part of the twentieth century. It has been shown that IR at medium doses (less than 3.0 kGy) can reduce or eliminate nonspore-forming pathogens such as Salmonella in food products including eggs (Farkas 1998).Although there are several publications related to the application of IR on eggs, a comprehensive review of the literature on this application is lacking. Therefore, the objective of this chapter is to collect the existing data and to review the effects of IR on the microbial population present in egg and on the quality, physicochemical, and functional properties of those products in order to evaluate the possibilities of obtaining shell-egg and egg products completely free of Salmonella contamination. To present the existing results more clearly, egg products have been grouped according to the preservation processes used: shell eggs, liquid eggs, dried eggs, and frozen eggs.

Ionizing Radiation of Shell-Eggs Dozens of publications have addressed the microbial lethal effect and properties impact of IR on shell-eggs.This commodity is a primary subject due to its importance as origin of foodborne illnesses and its large market share (69% of the total egg consumption). However, there remain unanswered questions in this field. Microbial Lethal Effect of Ionizing Radiation on Shell-eggs The antimicrobial efficacy of IR on shell-eggs depends fundamentally on three different factors: (1) the localization of the microorganisms, that is, on the shell vs. inside the egg; (2) the microorganism investigated; and (3) the irradiation source (Table 12.1). Bacteria isolated inside the egg show

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a higher resistance to IR due to the protective effect of the shell. Thus, Salmonella serovar Enteritidis showed D10 values of 0.27, and 0.20 kGy when it was inoculated inside or on the surface of the egg, respectively (Tellez and others 1995;Verde and others 2004). From the results in the literature, it has been indicated that Salmonella serovar Typhimurium was the most IR-resistant pathogenic microorganism. Based on these results, radiation doses of 1.5 kGy, using photon sources such as x-rays or gamma rays, have been proposed to be sufficient to render eggs free of pathogenic microorganisms such as Salmonella, Listeria monocytogenes, and Campylobacter jejuni (Serrano and others 1997; Verde and others 2004). However, the overall microorganisms of the egg display a higher IR resistance of D10=1.39 kGy.Also of concern, electron beam irradiators (EBI), due to the lack of penetration into a dense medium such as shell eggs, have been shown to be ineffective even at doses of 3 kGy (Wong and Kitts 2002).Therefore, the experimentally optimal dose of 1.5 kGy, when applied under commercial conditions using EBI, was not able to obtain safe and stable shell-eggs by IR treatments. Based on studies by E.S. Josephson (FDA Fed. Reg. 65, 2000) in the areas of radiation chemistry, nutrition, toxicology, and microbiology of shell-eggs, the US-FDA approved the use of up to 3 kGy ionizing radiation dose to reduce the level of Salmonella in fresh shell-eggs. However, it should be noted that these high doses could affect internal quality, physicochemical characteristics, and functional properties of fresh eggs, a point that is discussed further later in this chapter. Internal Quality of Ionizing Radiated Shell-Eggs The chemical content and details of egg physical composition, such as lipid profile and high water and protein content, create an environment conducive to the formation of volatiles during processing that could affect its quality properties. Changes in Haugh unit, color, and flavor of IR eggs have been detected. IR at any dose resulted in a significant decrease in Haugh unit (Tung and others 1970;Tellez and others 1995; Ma 1996), observing reductions up to 80% at 3 kGy (Ma and others 1990) or even higher when IR eggs were stored at 4°C for several days (Wong and Kitts 2002). When treated with gamma radiation as an individual treatment, the sensory quality of eggs classified as grade A, using USDA standards, was reduced to grades B and C by doses of 0.4 and 1.5 kGy, respectively (Tung and others 1970).The main reason for the loss of egg white quality associated with a decrease in Haugh unit is due to the irradiationinduced rupture of the albuminous sac and the subsequent loss of thick albumen, which could be caused by the irradiation-induced scission of

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Figure 12.1.

Food Irradiation Research and Technology

Eggs treated at different gamma irradiation doses.

O-glycosides from the ovomucin protein moiety. Figure 12.1 shows eggs treated at different gamma irradiation doses. Doses as low as 0.5 kGy already induced clearly visual modifications, with changes becoming increasingly noticeable as dose increases. IR also induces color changes. The yellow color of yolk became pale and the white egg was modified to a turbid yellow (Pinto and others 2004). These alterations were dependent on the irradiation source and dose. Insignificant differences between non-IR and IR egg were observed

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under 1.5 (Serrano and others 1997), 2 (Ma and others 1990; Pinto and others 2004), and 4 kGy (Wong and Kitts 2002) when X-rays, gamma rays and EBI were used, respectively.At any case, the higher the applied dose, the greater the loss of yolk color intensity (Tellez and others 1995). Oxidation of carotenoids is a likely cause of the discoloration of egg yolk (Katusin-Razem and others 1989). A definite off-odor in treated eggs was detected by using gamma irradiation at doses as low as 0.97 kGy (Ma and others 1990) due to oxidation of polyunsaturated fatty acids (Thakur and Singh 1994). However, off-flavor was not detected after the application of EBI to shell-eggs at 2–4 kGy (Wong and Kitts 2002). More studies are necessary to clarify this point and to determine the actual lipid oxidation impact by using other, more penetrating IR sources. Physicochemical Properties of Ionizing Radiated Shell-Eggs Depending on the dosage, IR can induce both direct (ionizing food constituents) and indirect (generating hydroxyl radicals that react with protein and lipid constituents) physicochemical changes in foods, thereby reducing both nutritional and functional properties (Thakur and Singh 1994). Egg pH and solid content were not affected by IR in either egg white or egg yolk (Ma and others 1990, 1994).The protein and SH contents of the white were also unchanged by IR; only a slight degradation of the higher molecular weight proteins was observed at 5 kGy (Pinto and others 2004). Although the albumen total protein content did not change breakdown and aggregation of the protein, secondary and tertiary structure was observed; these effects were seen as alterations of the major egg white proteins conalbumin, ovalbumin, and specially ovomucin, which contributes to the gel-like structure of thick white (Ma and others 1990; Wong and Kitts 2002). In the case of egg yolk, increasing the radiation doses leads to increasing losses of protein and SH contents, up to 2% and 1% losses, respectively, at 2.98 kGy. This suggested some breakdown of proteins in egg yolk, aggregation and partial denaturation of lipoproteins, transitions of SS linkages to free SH groups, or SH oxidation in the yolk proteins. The changes in albumen and yolk proteins would explain the progressive decrease in viscosity of the egg white with increases in the level of radiation, and the increment of the viscosity of egg yolk starting at 2.37 and 2.98 kGy (Ma and others 1994). However, because the changes in viscosity are more pronounced in egg white, which constitutes the major portion of shell-egg mass, this loss of viscosity is carried over into liquid whole egg (LWE) products derived from irradiated shelleggs (Ma and others 1990).

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Functional Properties of Ionizing Radiated Shell-Eggs Eggs serve many important roles in food products owing to their functional properties (foam formation, emulsification, and gelling). Formation of protein foams and emulsions depends on partial denaturation of protein at air-liquid and oil-water interfaces, respectively. The capability of the unfolded protein to form an elastic layer at the interface determines the foam stability. Following gamma radiation of shell-eggs up to 2.98 kGy, the altered conformation of proteins from egg white, the lowered viscosity, and the higher surface hydrophobicity increased both foaming and emulsion formation and stabilization (Ma and others 1990, 1994). In contrast, Wong and Kitts (2002) observed that when EBI was used, dosages of up to 4 kGy did not significantly affect the foaming capacity, and foam stability decreased at all IR doses.This different behavior could be due to a minor denaturation of proteins obtained with EBI in shell-eggs. The ability of eggs to form gels upon heating is the underlying reason for their usage as a binding agent in foods. Results obtained in the egg white gel hardness after IR of shell-eggs also depended on the IR source used. Although Ma and others (1990) observed a significant increase in firmness of heat-formed gel at 0.97 and 2.37 kGy by using gamma irradiation, Wong and Kitts (2002) determined that firmness decreased between 2 and 4 kGy EBI. Based on the above results, the doses (that is, up to 3 kGy) proposed by FDA would enable processors to obtain a product free of Salmonella serovar Enteritidis, but with compromised properties of the fresh egg, especially on the internal quality. The apparent change in egg quality and mainly the loss of white consistency after the egg is broken could result in consumer rejection of IR fresh shell-eggs, despite the increased safety of the product.However,from a different point of view more concerned with eggs as a processed food ingredient, the IR-induced quality modifications could be an advantage, due to enhanced foaming and emulsifying properties after IR. In addition, IR-induced white-yolk difference in viscosity would facilitate separation, and the global decrement of viscosity would make easier the pumping of LWE in factory equipment. Decreased viscosity would also increase the heat transmission coefficient, reducing the duration of the heating-up phases of possible posterior heat treatments. Ionizing Radiation of Refrigerated Liquid Egg Refrigerated liquid egg products represent 65% of the global production of egg products. Of this market segment, 60% corresponds to LWE,

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25% to egg white, and 15% to egg yolk. In order to present the results from literature more easily, this classification is followed. Ionizing Radiation of Liquid Whole Egg There are hardly any investigations related to the effect of IR treatments on LWE despite its important market. Literature dated from the 1950s and 1960s was only tangentially related to the lethal effect of IR on Salmonella and to the IR impact on the color and flavor. Microbial Lethal Effect of Ionizing Radiation in LWE Early studies from Proctor and others (1953) indicated that Salmonella serovar Typhimurium was most IR resistant (refer to Table 12.1). Doses of 2.5 kGy applied with a 3 MeV Van de Graaff generator caused a reduction of 6 log10 cycles of the population of this microorganism. More recent investigations also showed a D10 value for Salmonella serovar Enteritidis of 0.26–0.27 kGy at room temperature, indicating a higher IR sensitivity than serovar Typhimurium (Schaffner and others 1989; Serrano and others 1997). However, it has been observed that Salmonella serovar Typhimurium was one of the Salmonella serovars most IR sensitive when LWE was treated with gamma radiation at 4°C (I. Álvarez, unpublished data). Quality of Ionizing Radiated LWE Nonsignificant differences in color have been observed between IR and non-IR samples up to a dose of 1.5 kGy (Serrano and others 1997). However, doses as low as 0.09 kGy resulted in a detectable off-flavor in IR LWE (Grim and Goldblith 1965).This off-flavor threshold dose could potentially be increased by reducing the degree of oxygen dissolved in the LWE through complete deaeration followed by nitrogen infusion (Labuza and others 1967). However, this approach has not been fully validated and therefore remains a topic for further investigation. Physicochemical Properties of Ionizing Radiated LWE Although no investigations have been undertaken concerning the direct effect of IR on physicochemical properties of LWE, information can be derived indirectly by a review of the properties of foodstuffs prepared using IR-treated LWE.The baking performance of sponge cakes has been pointed out as a highly sensitive index to destructive changes in the quality of egg protein as well as to changes in the colloidal state of the emulsion of yolk lipid material (Proctor and others 1953). Investigations indicated that sponge cakes made from eggs irradiated at 2.5 kGy were

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comparable to cakes made from non-IR samples, with respect to volume, texture, and organoleptic qualities. Based on the above results, doses between 2–2.5 kGy would be necessary to obtain a Salmonella-free LWE, but with the previously noted undesirable changes in physiochemical properties.The relatively scant body of literature on the effect of IR on the microbial lethality and properties of LWE, and the relatively large potential market of this product, offer a wide field for research in order to establish IR doses that make it possible to obtain a safe and stable product with the properties as good, or perhaps better than, heat-pasteurized LWE. Ionizing Radiation of Liquid Egg White Egg white is 88% water and 11% proteins, and is a much more sensitive product to heat than is LWE. Denaturing of the least stable proteins of albumen begins at temperatures as low as 57°C (Johnson and Zabik 1981), affecting their functionalities in a negative manner. Therefore, ionizing radiation could be an alternative process for this product. Microbial Lethal Effect of Ionizing Radiation in Egg White Doses of 2.5 kGy were enough to produce a 10 log10 destruction of Salmonella serovar Typhimurium and even greater reductions of Salmonella serovar Senftenberg (refer to Table 12.1). Quality of Ionizing Radiated Egg White The whiteness of egg white decreased with the dose, being more significant at doses over 2 kGy. IR egg white had a transparent, dull, greenishyellow color (Ball and Gardner 1968; Pinto and others 2004). Physicochemical Properties of Ionizing Radiated Egg White Egg pH and solid content were not affected by IR up to doses of 2.98 kGy (Ma and others 1994).The protein content was also unchanged. However, different investigations indicated that egg proteins were aggregated by ionizing radiation at doses of 1.5 kGy (Hajós and others 1990; Kume and others 1994; Kume and Matsuda 1995). Also, the production of lowmolecular-mass components (30 kDa) was induced by doses of 2 kGy and, more notably, at 10 kGy.This would suggest that IR induced peptide bond cleavage resulting in the production of degraded fragments of eggwhite proteins such ovalbumin, ovotransferrin, and ovomucoid. The formation of these breakdowns could explain the decrease of the viscosity of IR egg white.

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Functional Properties of Ionizing Radiated Egg White Egg white treated at 3.8 kGy yielded albumin foams with marked differences in foam stability from the nontreated ones. However, flavor tests and volume of angel cakes prepared from IR and non-IR egg whites showed, in general, nonsignificant differences or a slight volume decrease (Nickerson and others 1957). Results appear to indicate that IR doses (2.5 kGy) causing a 10 log10 reduction in Salmonella induce minor deteriorations in the functional properties, but noticeable modifications could be observed especially on the quality and physicochemical properties of egg whites. Ionizing Radiation of Liquid Egg Yolk Egg yolk is used more as an ingredient in the preparation of other products due to its excellent properties as an emulsifier. This is the primary reason for the focus on functional properties, rather than microbial safety, in studies of the effect of IR on egg yolk. Data related to the microbial lethal effect of IR on egg yolk are almost entirely lacking. However, the safety and security of ingredients, and especially egg yolk that is associated with Salmonella contamination, should be considered because they can also be a source of foodborne bacteria and a causal agent in foodborne illness. Quality of Ionizing Radiated Egg Yolk IR induced discoloration of the egg yolk (Brooks and others 1959; Ma and others 1990).This effect was IR-dose dependent and was more significant for doses above 2 kGy (Pinto and others 2004).The color change could have been caused by the destruction of carotenoids in egg yolk, whose decay was proportional to the radiation dose (Katusin-Razem and others 1992). Physicochemical Properties of Ionizing Radiated Egg Yolk The pH of egg yolks treated at 2.5 kGy (pH 5.86) was significantly higher than that of nonprocessed ones (pH 5.79). Doses up to 5 kGy had minimal influence on the protein content or phospholipid degradation of the egg yolk (Huang and others 1997; Pinto and others 2004). Only a 0.5% loss in soluble protein content was observed, most probably caused by radiation-induced changes resulting in less soluble aggregates in egg yolk. Functional Properties of Ionizing Radiated Egg Yolk IR egg yolk had a significantly higher emulsion capacity than nonprocessed yolks. This improvement could have been due to the partial

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protein denaturation and exposed hydrophobicity of proteins (Huang and others 1997). The scant data related to IR on egg yolk would indicate that for liquid egg yolk products, IR at dosages of 2.5 kGy would not significantly affect the physicochemical properties and would, in fact, marginally improve the egg yolk functional properties. However, more studies are necessary to determine whether the indicated dose would be sufficient to offer a safe product and whether that dose would not infer any quality deterioration of egg yolk, especially with regard to flavor.The yolk’s high content of lipids, particularly unsaturated lipids, which are very reactive in radical induced chain reactions, is a potential source of objectionable flavor components.

Ionizing Radiation of Dried Egg Dried egg, which represents 25% of egg product production, is widely used by the food industry in bakery products, numerous semi-prepared products, ice creams, and others. Due to the dry state of this egg product, available water is reduced for chemical reactions and the IR-induced radiolysis of water is minimized. Dried egg is therefore a suitable product for IR treatment. Microbial Lethal Effect of Ionizing Radiation in Dried Egg IR doses of 2.4–2.0 kGy have been suggested to be adequate for a Salmonella inactivation factor of 103 considering D10 values in the order of 0.6–0.7 kGy for a mixture of Salmonella strains (Katusin-Razem and others 1992). Narvaiz and others (1992) obtained a D10 value of 1.0 kGy when determining IR resistance of natural Salmonella flora.This would indicate that initial doses did not reduce Salmonella in dried egg to the desired “nondetectable” level. However, with post-IR (2 kGy) storage of 20 days at 20° C, an absence of natural Salmonella flora in 25 grams was demonstrated. Quality of Ionizing Radiated Dried Egg The color of dried whole egg fades as a function of the dose, in treatments up to 2 kGy (Narvaiz and others 1992). For yolk egg powder, the threshold dose for color reduction was estimated at 1.5 kGy (Ferreira and del Maestro 1998).As it was pointed out in the case of shell-eggs and egg yolk, the destruction of carotenoids by hydroperoxidation is a likely cause of the discoloration.

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Sensory evaluation of egg powder irradiated in the presence of air resulted in detectable off-flavors following treatment with 4 kGy or more (Katusin-Razem and others 1989). As previously indicated, the flavordifference threshold dose for LWE was found to be around 0.09 kGy.This would indicate an advantage of IR egg in the dry state. Physicochemical Properties of Ionizing Radiated Dried Egg Neither pH nor solid content was significantly changed by IR up to doses of 8 kGy (Ma and others 1994).The relationship of viscosity to dose was nonlinear, with a threshold value observed at 5 kGy.Viscosity determinations indicated that viscosity changed more rapidly following doses over 5 kGy (Narvaiz and others 1992; Ferreira and del Maestro 1998).A mechanism for the nonlinearity of response was not proposed. Five kGy or higher doses were also necessary in order to observe significant radiation-induced loss of amino acids, such as of methionine, hystidine, tyrosine, and lysine (Katusin-Razem and others 1989). The resulting damage to the amino acids must be due to both the direct effect of IR and to radical transfer to amino acid residues with long reactive side chains and groups. Although the dry state protects the egg against flavor deterioration, the amount of unsaturated fatty acids in yolk lipids and the unfavorably high surface-to-volume ratio render dehydrated egg products significantly more susceptible to peroxidation (Addis 1986). Peroxidation products in foods are equally undesirable from the standpoint of toxicity (Kaneda and Miyazawa 1987), as well as palatability (St.Angelo and Bailey 1987). An induction dose of 2.5 kGy was observed in air in both whole egg powder and egg yolk powder (Katusin-Razem and others 1992). Removal of oxygen resulted in a significant reduction of the amount of lipid hydroperoxides formed. Functional Properties of Ionizing Radiated Dried Egg Doses of 2 kGy had no significant impact on foam formation or stabilization of IR powder whole egg (Narvaiz and others 1992). In contrast, foaming and emulsifying properties of dried-egg white increased with IR, and gel hardness decreased at 2 kGy but was not affected at 5 and 8 kGy (Ma and others 1994, 1996). Sponge cakes made with whole egg powder treated at 2 kGy (Narvaiz and others 1992) and angel cakes prepared with IR powder-egg white also at 2 kGy (Ma and others 1994) were not different in volume, flavor, or texture from those made with the non-IR egg products.

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The effects of ionizing radiation in aqueous products correspond mainly to their reactivity with the reactive species from the radiolysis of water; therefore, this mechanism of action is reduced in a solid dry system such as egg powder.Thus, higher doses are required to observe any effect on different parameters. From the aforementioned results, dried eggs treated with 2 kGy, preferably followed by storage at room temperature, would enable the production of a Salmonella-free product, with even better properties than the conventionally heat-processed ones. Furthermore, IR of dried egg products could be both less energy and time consuming than the heat process. Glucose must be removed before heating in order to prevent a Maillard reaction, which also may lead to a further proliferation of Salmonella during fermentation for glucose removal.The simplification of the preparation of the dried egg products intended for IR treatment would suggest economic benefit for IR-processed material.

Ionizing Radiation of Frozen Egg Frozen eggs represent 10% of egg product production. However, in current industrial practice this percentage is progressively decreasing due to the significant modifications of functional properties caused by freezing (especially yolk gelling). Similar to dried eggs, because most of the egg water is not available to participate in IR-induced radiolysis of water, frozen egg could be also an appropriate product to be treated by this technology. Microbial Lethal Effect of Ionizing Radiation in Frozen Egg Frozen whole egg is frequently contaminated with Enterobacteriaceae. D10 values (-18° C) ranging from 0.39 to 0.77 kGy have been determined for Salmonella, 0.52 kGy for E. coli, and 0.26 kGy for other Enterobacteriaceae (Brooks and others 1959; Comer and others 1963; Kijowski and others 1994; Fengmei and others 2000). Nevertheless, the effect of radiation dose on mesophilic aerobes is less pronounced. This would indicate that the recommended doses to reduce Enterobacteriaceae (2.5 kGy) would be a useful tool also for improving the hygienic status of frozen whole eggs. Physicochemical Properties of Ionizing Radiated Frozen Egg Little information is available related to the IR effect on physicochemical properties of frozen whole egg. Investigations indicate that nonsignifi-

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cant differences are observed in contents of lipids and proteins, amino acids, vitamins A, B1, and B2, carotenes, and viscosity between the non-IR frozen egg liquid and that treated at doses of 2 kGy (Fengmei and others 2000). IR doses of 4 kGy had a similarly nondetectable effect on the pH, percentage of solids, and protein content in IR frozen egg white and frozen egg yolk (Ma and others 1994). However, the SH content decreases with increasing doses, along with the induction of aggregation of globular proteins that probably were held together by disulphide linkages and covalent crosslinks (Hajós and others 1990). Functional Properties of Ionizing Radiated Frozen Egg Doses of up to 4 kGy had only slightly increased the hardness of thermal gel prepared with IR frozen whole egg and frozen egg white (Kijowski and others 1994; Ma and others 1994). In contrast, foaming and emulsifying properties decreased by 4% and 20%, respectively, at 2.5 kGy, and in both cases 20% at 4 kGy (Ma and others 1994). Sensory tests of sponge cakes made using irradiated (5 kGy) frozen whole egg, or angel cakes made using irradiated (4 kGy) frozen egg white, appeared to be somewhat improved or not significantly different from cakes prepared using non-IR egg ingredients (Nickerson and others 1957; Kijowski and others 1994). Apart from the possibility that IR could improve the microbiological quality of the egg in the frozen state, the manufacture of frozen egg could be particularly suited to IR processing in the final container.The material (frozen eggs) inevitably spends a considerable time in frozen storage before sale, allowing the continuous, and hence efficient, utilization of an ionizing radiation facility. However, a problem that could be associated with the IR of frozen eggs is that the radiolytic products that have been trapped and immobilized in the frozen, solidified egg material may undergo further reactions (for example, an increased intensity of lipid oxidation) during thawing at ambient temperatures (Kijowski and others 1994). The results presented up to this point indicate that IR could allow the production of eggs and egg products free of pathogenic microorganisms, thereby improving their hygienic status. However, doses required to obtain IR-pasteurized egg products would result in inferior sensory properties in comparison to nonirradiated products.Table 12.1 summarizes the existing data concerning microbial resistance to IR in shell-egg and egg products, and Table 12.2 the effects on their quality, physicochemical and functional properties when IR was applied at pasteurization doses.

212

Van de Graaff (3 MeV) EBIg Cobalt-60 (0.039 kGy min-1) Cobalt-60 (0.039 kGy min-1) Cesium-137 (0.089 kGy min-1) Cesium-137 (0.089 kGy min-1) Cesium-137 (0.089 kGy min-1) EBIg (10 MeV; 8.1kW)6 Van de Graaff (3 MeV) Van de Graaff (3 MeV) Cobalt-60 (0.08580 kGy min-1) Cobalt-60 (0.024 kGy min-1)

N.I.f Room Temperature 19 60 4 4 4 2 N.I.f N.I.f Room N.I.f Room Temperature Room Temperature

0.42 0.27 0.26 0.08 0.49 0.65 0.44 0.36 0.21 0.13 1.0 0.8 0.4 0.4

Van de Graaff (3 MeV) Van de Graaff (3 MeV)

EBIg (10 MeV; 60 kW) Cobalt-60 (0.017 kGy min-1) Cobalt-60 (0.017 kGy min-1) Cobalt-60 X-rays EBIg (10 MeV; 60 kW) EBIg (10 MeV; 60 kW) Cobalt-60 (0.017 kGy min-1)

IR Source

N.I.f Room Temperature Room Temperature N.I.f Room Temperature N.I.f N.I.f Room Temperature

Temperature (ºC)

0.81 0.31 0.204 0.27 0.32 0.76 0.53 0.082

D10 (kGy)

S. typhimurium S. typhimurium S. enteritidis S. enteritidis S. enteritidis L. monocytogenes E. coli Campylobacter jejuni LWEc S. typhimurium LWEc S. enteritidis LWEc S. enteritidis LWEc S. enteritidis LWEc S. enteritidis LWEc S. senftenberg LWEc S. typhimurium Liquid egg white S. typhimurium Liquid egg white S. typhimurium Liquid egg white S. senftenberg DWEd Natural Salmonella flora DWEd S. typhimurium, enteritidis and lille Dried egg white S. typhimurium Dried egg white S. senftenberg

Microorganisms

Nickerson and others 1957 Nickerson and others 1957

Matic and others 1990

Proctor and others 1953 Serrano and others 1997 Schaffner and others 1989 Schaffner and others 1989 Álvarez unpublished data Álvarez unpublished data Álvarez unpublished data Wong and others 1996 Nickerson and others 1957 Nickerson and others 1957 Narvaiz and others 1992

Wong and Kitts, 2002 Verde and others 2004 Verde and others 2004 Verde and others 2004 Serrano and others 1997 Wong and Kitts 2002 Wong and Kitts 2002 Verde and others 2004

Reference

Microbial Resistance to Ionizing Radiation in Egg and Egg Products (In All Cases, the Atmosphere Was Air)

Shell-egg (IC)a Shell-egg (EC)b Shell-egg (EC)b Shell-egg (IC)a Shell-egg (IC)a Shell-egg (IC)a Shell-egg (IC)a Shell-egg (IC)a

Product

Table 12.1.

213

E. coli Salmonella spp.

FWEe FWEe

b

Shell-egg (IC): Shell egg internally contaminated Shell-egg (EC): Shell egg externally contaminated c LWE: Liquid whole egg d DWE: Dried whole egg e FWE: Frozen whole egg f N.I.: non indicated g EBI: Electron beam irradiator

a

Salmonella spp.

FWEe

Frozen egg white S. typhimurium Frozen egg white S. senftenberg

Microorganisms 0.39 – 0.77 0.52 0.36 – 0.54 0.14 0.11

D10 (kGy)

–28.9 –28.9

–18 –15

–18

Temperature (ºC)

Van de Graaff (3 MeV) Van de Graaff (3 MeV)

Cobalt-60 (0.11 kGy min-1) Cobalt-60 (0.0818 kGy min-1)

Cobalt-60 (0.11 kGy min-1)

IR Source

Nickerson and others 1957 Nickerson and others 1957

Kijowski and others 1994 Comer and others 1963

Kijowski and others 1994

Reference

Microbial Resistance to Ionizing Radiation in Egg and Egg Products (In All Cases, the Atmosphere Was Air) (continued)

Product

Table 12.1.

214

2.5

2

2.5

Egg-yolka

DWEb

FWEc

—

—

—

d

—

d

Haugh unit

—

d

Transparent, dull greenish, yellow color Discoloration

Yolk: pale yellow White: turbid yellow —

Color

—

NAe

—

—

Off-flavor

Off-flavor

Flavor

b

Refrigerated LWE (liquid whole egg), egg-white or egg-yolk DWE: Dried whole egg c FWE: Frozen whole egg d DW: dried white e NA: Non-affected

a

2.5

Egg-whitea

2 – 2.5

3

Shell-egg

LWEa

Dose (kGy)

Quality Properties

NAe

NAe

c

—

c

NAe

d

—

d

NAe

—

NAe

pH Viscosity

NAe

NAe

NAe

NAe

—

NAe

Solid Content Lipids

NAe

NAe

Aggregation

Aggregation breakdown

—

—

NAe

—

—

Oxidation

Aggregation Oxidation breakdown

Proteins

Physicochemical Properties

c

Emulsifying

IR source dependence

Gelling

Sponged cakes made from IR LWE were similar to those prepared with non-IR LWE Angel cakes made from IR white were similar to those prepared with non-IR white — c — NA4 (DWEb) — — c (DWd) c (DWd) d (DWd) Sponged and angel cakes made from IR egg were similar to those prepared with non-IR egg d d NAe Sponged and angel cakes made from IR egg were similar to those prepared with non-IR egg

c

Foaming

Functional Properties

Influence of Ionizing Radiation at Pasteurizing Doses in the Properties of Egg and Egg Products

Product

Table 12.2.

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Strategies to Increase the Quality of Irradiated Egg Products Two possible approaches can be followed in order to overcome the unwanted effects of IR in egg products. First, increase the radiation tolerance of the product. Second, develop a means to increase the radiation sensitivity of the target pathogens (Borsa and others 2004). Increasing the degree of radiation tolerance of the product can be achieved by a number of strategies, including the addition of antioxidants, the exclusion of oxygen, or the reduction of the available water content of the product. Products that have low water availability, for example, dried and frozen egg products, could be suitable for irradiation treatment. Microbial radiation sensitivity can be increased by affecting the microbial homeostasis or by inducing sublethal damage, which are crucial aspects for combined processes. IR can induce stress in the microorganisms and thus provide new opportunities for designing combined processes with additional or synergistic effects. Several technologies in combination with IR have been tested in distinct products (heat, lowtemperature and modified atmospheres, high hydrostatic pressures, chemical preservatives) (Raso and Barbosa-Cánovas 2003). In egg products, irradiation has been combined most commonly with heat treatments. Controlled heating followed by IR significantly decreased IR D10 values. However, this reduction was very small and the processing time required was excessive, making the process of heating prior to IR not very feasible using current treatment protocols. On the other hand, when heat treatment and IR were simultaneously applied (thermoradiation), bacterial destruction was significantly enhanced (Licciardello 1964; Schaffner and others 1989). Thermoradiation caused greater inactivation of Salmonella serovar Enteritidis in LWE than heat or IR alone, or IR followed by heat, reducing the IR D10 value from 0.26 at 19°C to 0.238 and 0.078 kGy at 50 and 60°C, respectively (Schaffner and others 1989). Although it has been observed that IR treatments reduced microbial thermal D values of posterior heat treatments in different products (Raso and Barbosa-Cánovas 2003), the data related to this combination in egg products is inconclusive.The sensitizing effect of IR to heat could make it possible to reduce pasteurization temperatures and times of egg products.This would conduct to potential energy, egg quality, and/or economic savings in egg-product production. It has been indicated that under some conditions a fraction of IR microorganisms were able to recover from a potentially lethal dose (Borsa and others 1995). Also, storage studies at cooling or freezing temperatures of IR egg products have shown a reduction of the number of survivors to IR treatments during the storage time (Matic and others 1990;

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Narvaiz and others 1992; Huang and others 1997;Wong and Kitts, 2002). This would suggest that ionizing radiation could induce a degree of sublethal cell damage that would be manifested as a microbial death during storage.This IR-induced cell damage opens the possibility to combine IR treatments with other preservation factors in order to apply lower IR doses than those previously indicated to obtain the same or higher safe security levels.

Areas for Future Research IR applied on eggs offers one possible means of obtaining safe and stable egg products.With current irradiation protocols, however, this safety and stability comes at the cost of reduced freshness properties and sensory quality. Because radiation-degradation of sensory quality is dose dependent (Sudarmadji and Urbain 1972), reduction of the treatment dose would result directly in improved sensory quality of the treated product. Therefore, more investigations related to the possibility of reducing the IR doses by combining different processes based on the homeostatic interference and the IR-induced damage have to be conducted.These combinations would be especially indicated for those egg products with high available water content. Because IR is known to induce changes in the antigenicity of egg proteins, another, less explored area for research is the use of IR to reduce the allergenicity of eggs (ovalbumin and ovomucoid, mainly). Results from literature (Kume and Matsuda 1995; Byun and others 2002; Kim and others 2002; Lee and others 2002) indicate that allergies induced by egg proteins could be effectively reduced by IR or by its combination with heat. However, the doses required are in the range of 8–10 kGy.Therefore, in order to open the possibility of offering low allergic foods, more investigations have to be done, specially orientated to reduce IR doses. Finally, the particular modifications that IR induces in egg proteins or lipids have become the bases for the detection, for purposes of regulatory compliance, of prior irradiation treatment of eggs and eggs products.Although physical (electron spin resonance), chemical (detection of long chain hydrocarbons or 2-alkylcyclobutanones), or immunological (detection of proteins or fraction of proteins) methods have been used for the detection of IR egg shell and egg products (Kume and others 1994; Kume and Matsuda 1995; Stevenson and Stewart 1995), additional study is necessary to standardize and validate the methods, or establish methods that are capable of providing an estimate of absorbed dose, or methods for the detection of IR egg added in foods.

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Conclusion With regard to eggs, the ultimate goal for producers, manufacturers, and food scientists is a treatment that results in eggs and egg products with nondetectable levels of harmful organisms, and similar and better sensory qualities, physicochemical attributes, and functional properties than conventionally processed products. Ionizing radiation is a promising technology for sanitation and preservation of shell-eggs and egg products, with particular promise for dried and frozen eggs. However, the existing literature is, in many cases, inadequate on the use of this approach as a standalone intervention. Basic research is required to establish treatment conditions and protocols using combinations of treatments that enable the elimination of pathogens, mainly Salmonella, while maintaining sensory attributes.

Acknowledgement The authors would like to thank the “Secretaría de Estado de Educación y Universidades” and the “Fondo Social Europeo” for a MEC/FULBRIGHT fellowship granted to I. Álvarez.

References Addis PB. 1986. Occurrence of lipid oxidation products in foods. Food Chem Toxicol 24:1021–1030. Anonymous. 2002. Salmonella Annual Summary 2002. National Center for Infectious Diseases. Division of Bacterial and Mycotic Diseases. Foodborne and Diarrheal Diseases Branch.Atlanta, Georgia 30333. Ball HR, Gardner FA. 1968. Physical and functional properties of gamma irradiated liquid egg white. Poultry Sci 47:1481–1487. Borsa J, Lucht L, Blank G. 1995. Recovery of microorganisms from potentially lethal radiation damage. Radiat Phys Chem 46(4-6):597–600. Borsa J, Lacroix M, Ouattara B, Chiasson F. 2004. Radiosensitization: enhancing the radiation inactivation of foodborne bacteria. Radiat Phys Chem 71:135–139. Brooks J, Hannan RS, Hobbs C. 1959. Irradiation of egg and egg products. Int J Appl Radiat Is 6:49–52. Bufano NS. 2000. Keeping eggs safe from farm to table. Food Technol 54(8):192. Byun MW, Lee JW,Yook HS, Jo C, Kim HY. 2002.Application of gamma irradiation for inhibition of food allergy. Radiat Phys Chem 63:369–370. Comer AG, Anderson GW, Garrad EH. 1963. Gamma irradiation of Salmonella species in frozen whole egg. Can J Microbiol 9:321–324. Doyle ME, Mazzotta S. 2000. Review of studies on the thermal resistance of Salmonellae. J Food Prot 63(6):779–795.

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Farkas J. 1998. Irradiation as a method for decontaminating food. Int J Food Microbiol 44:189–204. Favier GI, Escudero ME, Mattar MA, de Guzmán AMS. 2000. Survival of Yersinia enterocolitica and mesophilic aerobic bacteria on eggshell after washing with hypochlorite and organic acid solutions. J Food Prot 63(8):1053–1057. FDA. 2000. Irradiation in the production, processing and handling of food. In: FDA Federal Register. 65(141):45280–45282. Fengmei L,Yongbao G, Dianhua C. 2000. Study on radiation preservation of frozen egg liquid. Radiat Phys Chem 57:341–343. Ferreira LFS, del Maestro NL. 1998. Rheological changes in irradiated chicken eggs. Radiat Phys Chem 52(1-6):59–62. Grim AC, Goldblith SA. 1965. The effect of ionizing radiation on the flavor of whole-egg magma. Food Technol 19(10):138–140. Hajós G, Kiss I, Halász A. 1990. Chemical changes of proteins of irradiated egg-white. Radiat Phys Chem 36(5):639–643. Huang S, Herald TJ, Mueller DD. 1997. Effect of electron beam irradiation on physical, physiochemical and functional properties of liquid egg yolk during frozen storage. Poultry Sci 76:1607–1615. Johnson TK, Zabik ME. 1981. Gelation properties of albumen proteins, singly and in combination. Poultry Sci 60:2071–2083. Kaneda T, Miyazawa T. 1987. Lipid peroxides and nutrition. World Rev Nutr Diet 50:186–214. Katusin-Razem B, Mihaljevic B, Razem D. 1992. Radiation-induced oxidative chemical changes in dehydrated egg. J Agr Food Chem 40:662–668. Katusin-Razem B, Razem D, Matic S, Mihokovic V, Kostromin-Soos N, Milanovic N. 1989. Chemical and organoleptic properties of irradiated dried whole egg and egg yolk. J Food Prot 52(11):781–786. Kijowski J, Lesnierowski G, Zabielski J, Fiszer W, Magnuski T. 1994. Radiation pasteurisation of frozen whole egg. In: Sim JS, Nakai S, eds. Egg uses and processing technologies. Wallingford, Oxon: CAB INTERNATIONAL, p. 340–348. Kim MJ, Lee JW,Yook HS, Lee SY, Kim MC, Byun MW. 2002. Changes in the antigenic and inmunoglobulin E-binding properties of hen’s albumin with the combination of heat and gamma irradiation treatment. J Food Prot 65(7):1192–1195. Kume T, Matsuda T. 1995. Changes in structural and antigenic properties of proteins by radiation. Radiat Phys Chem 46(2):225–231. Kume T, Ishii T, Matsuda T. 1994. Immunochemical identification of irradiated chicken eggs. J Sci Food Agr 65:1–4. Labuza TP, Goldblith SA, Chandler EL. 1967. Radiation-induced off-flavor development in whole-egg magma. J Food Sci 32:61–63. Lee JW, Lee KY,Yook HS, Lee SY, Kim HY, Jo C, Byun MW. 2002. Allergenicity of hen’s egg ovomucoid gamma irradiated and heated under different pH conditions. J Food Prot 65(7):1196–1199. Licciardello JJ. 1964. Effect of temperature on radiosensitivity of Salmonella Typhimurium. J Food Sci 29:469–474. Ma CY. 1996. Effects of gamma irradiation on physicochemical and functional properties of eggs and egg products. Radiat Phys Chem 48(3):375. Ma CY, Sahasrabudhe MR, Poste LM, Harwalkar VR, Chambers JR, O’Hara KPJ. 1990. Gamma irradiation of shell eggs. Internal and sensory quality, physicochemical characteristics, and functional properties. Can Inst F Sci Tec J 23(4/5):226–232.

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Ma CY, Sahasrabudhe MR, Poste LM, Harwalkar VR, Chambers JR, O’hara KPJ. 1994. Gamma irradiation and physicochemical properties of eggs and egg products. In: Sim JS, Nakai S, editors. Egg uses and processing technologies. Wallingford, Oxon: CAB INTERNATIONAL, p. 283–300. Mañas P, Pagán R, Álvarez I, Condón S. 2003. Survival of Salmonella senftenberg 775W to current liquid whole egg pasteurization treatments. Food Microbiol 20:593–600. Matic S, Mihokovic V, Katusin-Razem B, Razem D. 1990.The eradication of Salmonella in egg powder by gamma radiation. J Food Prot 53(2):111–114. Narvaiz P, Lescano G, Kairiyama E. 1992. Physicochemical and sensory analyses on egg powder irradiated to inactivate Salmonella and reduce microbial load. J Food Safety 12:263–282. Nickerson JTR, Charm SE, Brogle RC, Lockhart EE, Proctor BE. 1957. Use of high-voltage cathode rays to destroy bacteria of the Salmonella group in liquid and frozen egg white and egg solids. Food Technol 11:159–166. Pinto P, Ribeiro R, Sousa L, Cabo Verde S, Lima MG, Dinos M, Santana A, Botelho ML. 2004. Sanitation of chicken eggs by ionizing radiation: functional and nutritional assessment. Radiat Phys Chem 71:33–36. Proctor BE, Joslin RP, Nickerson JTR, Lockhart EE. 1953. Elimination of Salmonella in whole egg powder by cathode ray irradiation of egg magma prior to drying. Food Technol 7:291296. Raso J, Barbosa-Cánovas GV. 2003. Nonthermal preservation of foods using combined processing techniques. Crit Rev Food Sci 43(3):265–285. Schaffner DF, Hamdy MK,Toledo RT,Tift ML. 1989. Salmonella inactivation in liquid whole egg by thermoradiation. J Food Sci 54(4):902–905. Serrano LE, Murano EA, Shenoy K, Olson DG. 1997. D values of Salmonella serovar Enteritidis isolates and quality attributes of shell eggs and liquid whole eggs treated with irradiation. Poultry Sci 76:202–206. St.Angelo AJ, Bailey ME. 1987.Warmed-Over Flavour of Meat. Orlando:Academic Press. Stevenson MH, Stewart EM. 1995. Identification of irradiated food: the current status. Radiat Phys Chem 46(4-6):653–658. Sudarmadji S, Urbain WM. 1972. Flavor sensitivity of selected animal protein to gamma irradiation. J Food Sci 37:671–672. Tellez IG,Trejo RM, Sanchez RE, Ceniceros RM, Luna QP, Zazua P, Hargis BM. 1995. Effect of gamma irradiation on commercial eggs experimentally inoculated with Salmonella serovar Enteritidis. Radiat Phys Chem 46(4-6):789–792. Thakur BR, Singh RK. 1994. Food irradiation—chemistry and applications. Food Rev Int. 10:437-73. Tung MA, Richards JF, Morrison BC. 1970. Rheology of fresh, aged and gamma-irradiated egg white. J Food Sci 35:872–874. Verde SC, Tenreiro R, Botelho ML. 2004. Sanitation of chicken eggs by ionizing radiation: HACCP and inactivation studies. Radiat Phys Chem 71:27–31. Wong PYY, Kitts DD. 2001. Factors influencing ultraviolet and electron beam irradiationinduced free radical damage of ascorbic acid. Food Chem 74:75–84. Wong PYY, Kitts DD. 2002. Physicochemical and functional properties of shell eggs following electron beam irradiation. J Sci Food Agr 83:44–52. Wong YC, Herald TJ, Hachmeister KA. 1996. Comparison between irradiated and thermally pasteurised liquid egg white on functional, physical and microbiological properties. Poultry Sci 75:803–815.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 13 IRRADIATION TREATMENT OF NUTS Akua Kwakwa and Anuradha Prakash

Introduction Nuts are a popular and valued global commodity. Pest infestation and contamination with mold (with resultant aflatoxin formation) are the major problems affecting the shelf-life, quality, and safety of nuts. Although contamination with pathogens is highly uncommon, recent outbreaks have prompted the nut industry to consider treatments to eliminate pathogens. Irradiation has the ability to treat both pest and microbial contamination.The characteristics, advantages, and disadvantages of irradiation treatment of nuts are discussed, as well as future research needed to provide information in the evaluation of irradiation as a potential cold pasteurization process. Nuts are highly valued components of cuisines worldwide for their unique flavors and textures. Nuts also contribute to nutritional value as important sources of unsaturated fatty acids, particularly the essential fatty acids linoleic acid (18:2) and linolenic acid (18:3), protein, and certain vitamins and minerals (International Tree Nut Council 1998; USDA 1984). They may be consumed raw or processed and combined with other ingredients in cereals, baked goods, snacks, confections, and meals. The United States holds a substantial 45% of the world market share of tree nuts. The United States is the largest commercial almond producer and exporter in the world, the second largest producer of walnuts, macadamia and pistachio nuts, and the third largest producer of hazelnuts (USDA-HTP 2004) and peanuts (International Tree Nut Council 1998). Contamination with nonpathogenic or pathogenic organisms leads to lowered quality and safety concerns, and a major loss of revenue for this highly valued commodity.

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Farming and Harvesting All nuts at maturity have a leathery outer hull, a thin shell, and an inner nut.Tree nuts have similar features at maturity:Their hulls split along their side, allowing the shell to dry and form a hard, protective shell around the nut. Walnuts and almonds are harvested using mechanical tree shakers that shake the nuts to the ground where they are raked into windrows and picked up by sweepers (Kader and Thompson 2002). Pistachios are shaken or knocked onto catching frames, or handpicked from the trees, but are not allowed to touch the ground because of their open shells and high moisture content (California Pistachio Commission 2005).

Insect Disinfestation Nuts are susceptible to pest damage including feeding, frass (fecal material), and webbing, which reduces their quality. Pests may infest the nuts on the tree, or when they come into contact with the ground during harvest (Table 13.1). Primary pests feed directly on the nuts, while secondary pests feed on fines or damaged nutmeats (UC Davis 2005). Pest damage is significantly reduced by fumigating the nuts with methyl bromide or phosphine immediately after harvest; this is repeated if they are stored for longer than six months.They may also be stored at cold temperature to reduce insect populations.After storage, they need an aeration period to remove any residue or chemical smell (Narvaiz and others 1992). Properly sealed packaging is also necessary to prevent reinfestation (Ahmed 2001). The USDA has specific tolerance limits for various nuts. For example, tolerance for insect damage, mold, rancidity, and decay is 1–2% for in-shell pistachio nuts and 0.3–0.5% for shelled pistachio nuts. No live insects are permitted in pistachios (USDA-AMS 2003a; USDA-AMS 2003b).

Microbial Contamination Contamination of nuts by yeast and mold is a concern because the aflatoxins generated have serious health consequences. Soil-based molds Aspergillus flavius and Aspergillus parasiticus frequently occur in peanuts. At sufficiently high amounts, they can produce aflatoxins that are detrimental to health and are regarded as carcinogenic (International Tree Nut Council 1998). High temperature and humidity during storage augment this damage (Chiou and others 1990). Rainfall during harvest and postharvest periods has shown to increase moisture and subsequent

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Table 13.1. Common Nut Pests and Their Symptoms (University of California at Davis 2005; 1: Johnson and Vail 1989; 2: Zalom and Bentley 1985; 3: Curtis and others 1983) Pest Name

Point of Infection

Navel Orangeworm “Mummy” nuts—nuts re(Amyelois transitella) maining on tree from previous crop3. New crop nuts. Later maturing nuts. Softshell almonds with a long hull split or poorly sealed shell. Indian Meal Moth Storage: secondary pests, (Plodia interpunctella) i.e., feed on fines and *Major pests of dried damaged kernels. fruits and nuts.

Southern Fire Ant (Tetramerium caespitum)

Peach Twig Borer (Anarsia lineatella)

Ground, especially in orchards with weeds, orchards without cover crop. Nuts with less tight shell seal, smaller shell splits, open shells. Almonds on young trees2. Growing shoots and nuts.

Damage Caused Bore into nutmeat. Later instars can consume most of the nut. Webbing and frass. Fungal infection of exposed nutmeat.

Feeding by larvae. Caking or crusting from webbing produced by larvae. Cast exoskeleton and frass. Repeated reproduction leading to damage by new generations1. Hollowed - out nutmeats. Chewing marks. White, dust-like remnants in nut2.

Chewing marks.

mold counts in walnuts (Wilson 1990) and nuts not dried following harvest may also be subject to mold infection. Absent or damaged shells can allow soil or dust contact to infect the nuts (International Tree Nut Council 1998). Coliforms, Escherichia coli, Streptococcus, Bacillus, Xanthomonas, Achromobacter, Psuedomonas, Micrococcus or Staphylococcus, and Brevibacterium have been isolated from almonds. Feeding by insects can also expose the nut meats to microbial damage (King and others 1970). On average, pistachios and peanuts have a mold contamination level of 1:5000 and 1:10000, respectively (International Tree Nut Council 1998). Mold counts on walnuts range from 100/g to 250,000/g, depending on rainfall conditions during harvest and postharvest handling and storage

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conditions. The industry standard is set at 5000/g, reinforcing the need for better control (Wilson 1990).

Contamination with Pathogens Recent outbreaks with microorganisms such as Salmonella Enteriditis (in almonds) have raised questions about the safety of raw nuts. Pathogen occurrence in nuts is not common, but contaminated nuts can cause serious illness or even death. Nuts may be contaminated with pathogens by various means such as contaminated water, use of inadequately composed manure, contamination by bird, squirrel, coyote, or other vertebrate fecal material, unsanitized and unclean harvesting and hulling equipment, exposure of the nuts to soil or high moisture, unclean and unsanitary restroom facilities, bad personal hygiene habits of employees, and almonds picked in the “wet” or “green” stage (University of California and Almond Board of California 2001). Bacteria are more likely to exist in immature almonds because of their high moisture content (Kiss 2002). Several studies have shown that nuts can be contaminated with Escherichia coli depending on the variety, source, and stage of harvest (Isaacs and others 2005). Contamination of almonds with coliforms, Escherichia coli, and Streptococcus was correlated to contact of nutmeat with soil especially during harvest (King and others 1970). Raw whole almonds and mixed snacks containing raw whole almonds provided by a U.S. supplier were recalled in April 2001 in Ontario, Canada, due to contamination with S. Enteriditis. The product was also implicated in a multistate outbreak in the United States (FDA 2002). This outbreak was traced to almonds produced in three orchards in California and contaminated with S. Enteriditis PT30, which has not been reported since 1992. In May 2004, a major almond producer in California instituted a voluntary recall when several people in multiple states were infected with Salmonella after consuming raw almonds.At least 13 million lbs of almonds were recalled and 29 people were hospitalized. The implicated organism was S. Enteriditis PT9c (CDC 2003). Thus, it is possible that raw nuts that are not treated further before consumption can be carriers of pathogens and pose a risk for susceptible populations. Treatment Options Most of the aforementioned sources of pathogenic and nonpathogenic contamination can be controlled through Good Manufacturing Practices

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(GMPs) and Good Agricultural Practices (GAPs) (Souza 2002). Effective measures for control of yeast and mold are rapid drying after harvest, correct atmospheric conditions for postharvest storage, transport and processing, removal of nuts with obvious mold contamination and nuts damaged by insects, and surface disinfection (for seed use) or fumigation (for pest control) (International Tree Nut Council 1998).

Pest Control Chemical fumigants are used for pest control. Methyl bromide is the most commonly used nut fumigant. It is a broad spectrum pesticide that allows horticultural products to meet Probit-9 specifications of 99.9968% pest elimination. It also disinfests these products in a timely manner (less than 24 hours) that allows exporters to be able to compete well with other international distributors (Aergerter and Folwell 2001). However, some pests, for example, P. interpunctella, have developed resistance (Ahmed 2001). In addition, methyl bromide has been linked to ozone depletion and toxic residual effects (Johnson and Vail 1989; Newsome 1987; Uthman and others 1998). Methyl bromide requires special handling by fumigation personnel, and residents located near areas of chemical application are susceptible to exposure by drift. Due to its lethal effects, the Clean Air Act was established in 1998 to phase out methyl bromide fumigation of commodities by 2005. Phosphine is a less costly alternative but requires 2–3 days plus aeration time.This puts U.S. exporters at an economic disadvantage in competing with other exporters. Propylene oxide treatment requires moisture and heat to be effective, but this can encourage mold growth. The effectiveness of this treatment depends on temperature and humidity of fumigation and the susceptibility of the particular organism (Wilson 1990). Controlled atmosphere consisting of low oxygen and/or high carbon dioxide is an effective disinfestation treatment but it takes 3–7 days plus an aeration period (Kader and Thompson 2002).

Pathogenic Microbial Control In addition to research on evaluating risk factors for pathogen growth and establishing guidelines for best practices, the nut industry, especially the almond industry, has initiated research to evaluate various treatments. Responding to the recent Salmonella outbreaks, the Almond Board of California (2004) has established the following criteria for any treatment to be approved for disinfection of almonds:

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• Identify the most resistant microbe of public health concern. • Have an appropriate performance standard. • Identify surrogates for use in testing and related performance standards; provide information on the resistance of surrogates and relevant pathogens. • Challenge studies should be conducted with Nonpareil almonds inoculated with 106–107 CFU/g, including specific test conditions, and describe recovery/ remuneration procedures. • Challenge studies must consistently achieve a 5-log reduction in Salmonella. • The treatment must be consistent for the entire surface of every kernel. • The general characteristics of the almond must be unaltered. • The process must not cause any negative health or safety concerns for consumers. • The system must have in-line process control, monitoring, and documentation devices. • The pasteurizer must be economical and easy to operate. At present, the Almond Board is evaluating thermal treatments (dry heat, moist heat [steam/air mixtures]) and nonthermal treatments such as cold plasma, ultra high hydrostatic pressure, ultrasound, ozone, controlled atmospheres, and chemical sprays.

Irradiation Treatment of Nuts Irradiation offers various advantages for disinfestation and pasteurization of nuts. The treatment can penetrate through the shell and provide homogenous treatment of the surface of the nut kernel. The process does not alter the general characteristics of raw almonds and does not raise the temperature of the kernel. Treatment can be performed on bulk almonds as well as within the final packaging.The dose levels used to control microbial pathogens will also control insect pests, mold, and other spoilage organisms.The FDA phytosanitary regulations (21 CFR 179.26) currently have an established limit of 1.0 kGy for disinfestation of arthropod pests although specific approval for irradiation treatment of nuts to treat microbial pathogens will require FDA approval.The National Food Processors Association (NFPA) in Washington, D.C., has filed a petition on behalf of the Food Irradiation Coalition that would allow ready-to-eat foods, including seeds and similar foods, to receive a dose of up to 7.0 kGy (FDA-HHS 2001). The petition will need an amendment to specifically include nuts.

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Insect Disinfestation The specific regulations on the use of irradiation as a phytosanitary treatment are discussed elsewhere in this book. It is generally accepted that 1 kGy treatment will eliminate most insects of significance in nuts by killing the insects (mortality), preventing emergence of adults, or inducing sterility. The Indianmeal moth, Plodia interpunctella, and the navel orangeworm, Amyelois transitella, are two major pests infecting nuts. Nonpareil almonds, Hartley walnuts, and Thompson seedless raisins were treated with irradiation doses from 0.144 kGy to 0.921 kGy to observe the effects on pupal mortality, adult fertility, and longevity, and subsequent mating success of the Indianmeal moth, Plodia interpunctella. Effects were the same for all food types. Up to 0.269 kGy, no significant reduction in adult emergence was observed. Between 0.594 and 0.607 kGy, adult emergence was significantly reduced. The emerging adults were weak, deformed, and unable to mate. At 0.822 kGy, more reduction was observed in adult emergence. The few that emerged were deformed and died soon after.At 0.921 kGy, no adult emergence was observed (Johnson and Vail 1987). Johnson and Vail (1989) also irradiated larvae of the Indianmeal Moth and the Navel Orangeworm at 0.337 Gy to 0.497 kGy and transferred them to the same nuts and fruits. No adult emergence was observed. The authors indicated that although radiation-induced mortality was delayed, damage to product quality was significantly reduced and overall appearance of the product was improved due to reduced webbing and frass.

Molds and Aflatoxins Contamination of tree nuts by aflatoxins produced after infection by the fungi Aspergillus flavus and Aspergillus parasiticus is a serious threat to human health (FDA/CFSAN 1992). The major aflatoxins of concern are designated B1, B2, G1, and G2.These toxins are usually found together in various foods and feeds in various proportions; however, aflatoxin B1 is usually predominant and is the most toxic.The current domestic guideline set by the FDA is 20 ng/g total aflatoxins but the European Community has instituted a standard of 2 and 4 ng/g aflatoxin B1 and total aflatoxins, respectively. In the United States, aflatoxins have been identified in peanuts and peanut products, and tree nuts such as Brazil nuts, pecans, pistachio nuts, and walnuts. Other nuts are susceptible but less prone to contamination (International Tree Nut Council 1998).

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Although irradiation can affect mold growth, it is not an effective treatment for destroying aflatoxins. English walnuts treated with gamma irradiation doses of up to 20 kGy had a greater decrease in mold counts as compared to propylene oxide–treated nuts. No significant differences were observed for yeast counts, which were < 10/g for all samples including the control (Wilson 1990). Changa and others (1988) treated walnuts with irradiation doses of 0.1 kGy to 1 kGy.A significant, though not complete, reduction in the number of kernels infested with Aspergillus sp. was observed. Other fungi were also not affected. Chiou and others (1990) inoculated peanuts with A. parasiticus NRRL 2999 and exposed them to irradiation up to 15 kGy. Five kGy and higher significantly reduced the outgrowth of A. parasiticus and naturally occurring mold, although complete elimination was not achieved at any dose level. Except for the samples irradiated at 2.5 kGy, all peanuts were highly contaminated with aflatoxin after four weeks of incubation; aflatoxin content was 69.12–13.48 μg/g, depending on the original irradiation dose. The elimination of competing molds may have given the surviving molds an opportunity to multiply rapidly, consequently creating large quantities of aflatoxins. Aziz and Moussa (2004) report that irradiation at 4.0 kGy reduced mold growth in groundnut seeds, no growth was observed at 5 kGy, and irradiation at 6.0 kGy detoxified aflatoxin B1 by 74.3–76.7%. Although mold growth and toxin formation can be inhibited by irradiation at 3–6 kGy, toxin inactivation requires much higher levels of treatment, especially in a dry medium.Temcharoen and Thilly (1982) indicated that a dose of 50 or 100 kGy was required to eliminate the effect of aflatoxin in peanut meal contaminated with aflatoxin.

Pathogen Inactivation There is little information on the efficacy of irradiation to treat microbial pathogens in nuts. Research has shown that most food pathogens are sensitive to irradiation (Ingram and Farkas 1976; Monk and others 1995). Campylobacter jejuni, A. hydrophia, Y. enterocolitica, Salmonella, Shigella, E. coli O157: H7, L. monocytogenes, and Staphylococcus aureus are among the microorganisms that have a low tolerance for irradiation. Spore-forming pathogens such as C. botulinum, C. perfringens, and Bacillus cereus are more resistant to irradiation (as they are to most processing technologies). Sensitivity of microbial cells to irradiation is a function of moisture content or water activity of the host product (and also relative humidity of the environment). Microorganisms are far more susceptible in high-moisture

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Table 13.2. Comparison of D values for Various Salmonella Strains in Different Food Products Strain

Medium

D Value

Reference

Salmonella Enteriditis

Orange juice

0.35–0.37 kGy

Salmonella Anatum

Orange juice

0.71 kGy

Salmonella cocktail

Broccoli seeds

1.11 kGy

Salmonella Lille, Enteritidis, Typhimurium Salmonella Mbandaka

Egg powder

0.8 kGy

Niemira and others 2001 Niemira and others 2001 Rajkowski and Thayer 2000 Matic and others 1990

Alfalfa seeds

0.81 kGy

Alfalfa seeds

0.98 kGy

Salmonella cocktail (4 strains)

Thayer and others 2003 Thayer and others 2003

environments. In low-moisture conditions such as in nuts, water molecules produce fewer radicals and thus have less indirect effects on the DNA of microbial cells.Table 13.2 shows the D value (dose required to decrease microbial counts by 90%) for Salmonella in various products.Thus a 5 log reduction of Salmonella in egg powder would require a dose of 4.0 kGy, and for broccoli seeds the necessary dose would be 5.55 kGy.

Chemical and Sensory: Irradiation Can Catalyze or Induce Lipid Peroxidation, and Lipid and/or Protein Radiolysis Lipid Peroxidation: Occurrence and Mechanism Lipid peroxidation is initiated when a hydrogen atom is abstracted from lipids at positions ␣ to the double bond in unsaturated fatty acids. The mechanism culminates in secondary oxidation products, such as aldehydes, ketones, esters, and acids. They are manifested as rancid/off-flavor and odors. Irradiation speeds up lipid peroxidation by forming lipid free radicals that react with oxygen, by breaking down hydro peroxides, and by destroying antioxidants (Nawar 1977). Nuts can be susceptible to lipid peroxidation and rancidity because of their high amounts of unsaturated fatty acids (Braddock and others 1995). Nuts with a high moisture content, soft texture, and no shell, such as peanuts, are more vulnerable to lipid peroxidation and degradation. Almonds and groundnuts have harder textures, shells present, and lower

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moisture content, and thus do not oxidize as easily (Sattar and others 1989). The physical form (whole or chopped) affects the surface area available for oxygen contact and therefore the extent of oxidation. Antioxidants and prooxidants affect susceptibility to peroxidation. Almonds contain 35.4 IU of vitamin E as ␣-tocopherol (USDA 1984).Their skins also contain 9 phenolic antioxidants (Sang and others 2002). The type of antioxidant also determines oxidative stability: ␣-tocopherol is one of the least resistant antioxidants to irradiation (Nawar 1977). O’Mahony (1985) performed sensory analysis of raw almonds irradiated at 100 krad (1 kGy) immediately after irradiation and after six months of storage. No significant sensory differences were detected, showing that irradiation up to 1 kGy did not induce off-flavors. Sensory rankings of raw almonds irradiated at 0.25, 0.5, 0.75, and 1.0 kGy were equal to or higher than rankings for the control almonds after two, four, and six months of storage.The control samples were ranked lower because of greater insect infestation (Sattar and others 1989). Pistachios irradiated up to 1 Mrad (10 kGy) had no off-flavor or rancidity, although their peroxide value was slightly increased after treatment (Thomas 1988). Uthman and others (1998) observed overall increase in value and variation of iodine number, peroxide value, and TBA values in irradiated raw almonds at 6 and 10.5 kGy.This suggests that lipid stability was affected. However, no GC or sensory analyses were performed. Walnuts were treated with gamma irradiation doses of 5, 10, 15, and 20 kGy, and compared to propylene oxide–treated nuts for microbial control (Wilson 1990). Free fatty acid values were not significantly different, and all values were below the maximum limit of 1%. Iodine value and TBA values were slightly reduced after irradiation and increased after propylene oxide treatment, although all values were still in a normal range. Peroxide value was significantly higher for irradiation-treated nuts. No rancidity or other off-flavor was detected in any of the samples, despite increases in peroxide values. Irradiation was more effective than propylene oxide at reducing microbial count. Santos (2001) did not observe a significant change in hexanal in almonds irradiated at 2 kGy and stored for 77 days. Hexanal also decreased in irradiated meat products (Jo and Ahn 2000; Nam and Ahn 2003; Shahidi and Pegg 1994), suggesting that irradiation does not necessarily induce lipid peroxidation in either high-fat or high-protein products. Shahidi and Pegg (1994) also suggest that hexanal may have reacted with other components or broken down to hexanoic acid. No sensory testing was done in these latter experiments to determine whether a rancid flavor was produced.

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Nonoxidative Radiolytic Reactions Irradiation can also induce protein and lipid radiolysis. Radiolysis reactions depend on a variety of factors such as the complexity of the food system, irradiation conditions, and product form (solid, liquid, or gas). Radiolysis reactions can occur concurrently with, or may even be favored over, lipid peroxidation. In lipid radiolysis, fatty acids are cleaved at one or more of four specific positions around the carboxyl groups.The resulting free radicals combine with hydrogen radicals or lose an excited portion to form stable products that are different from the parent lipid. The stable products are mostly alkenes and a few aldehydes (Nawar 1978; Miyahara and others 2002). Protein radiolysis can result in strong off-flavors when sulfur containing amino acids are broken down into sulfur-containing volatiles such as dimethyl sulfide, dimethyl disulfide, dimethyl trisulfide, and methane thiol (Ahn 2002; Urbain 1977). The odor has been described as “bloody and sweet” or “burnt oil” in meats (Ahn and others 2000), and “bitterness” or “medicinal” in orange juice (Spoto and others 1997). Kwakwa (2003) irradiated Nonpareil almonds up to 15.20 kGy. Sensory acceptability by a trained sensory panel started to decline after 4 kGy, and the almonds were judged to be completely unacceptable at 15.20 kGy. Although GC/MS showed an increase in lipid oxidation products, the dominant offflavor was different from a rancid flavor, suggesting protein radiolysis. Almonds contain about 20% protein (Almond Board of California 1998); therefore, protein radiolysis is likely. Further research requires a combination of sensory studies, analytical detection, and quantification of protein radiolysis end products. This will provide critical information in setting realistic irradiation dose ranges for nuts so that the sensory quality is not compromised. Advantages of Using Irradiation to Treat Nuts • Treatment can be performed on bulk almonds as well as post-packaging. • The penetrative depth makes irradiation particularly effective for inshell nuts. • Processing can be configured to achieve uniform treatment of every kernel. • The process also does not raise the temperature of the kernel. • No residues remain in the treated product. • The dose levels used to achieve 5 log reduction of Salmonella will also control insect pests,mold,and other pathogens of concern such as E.coli.

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• Equipment and facilities are available for treatment. • Depending upon volume, cost of irradiation can be competitive with other treatments. Research Needs At this time, research is needed to determine effective dose levels to achieve 5 log reductions of target organisms, especially Salmonella spp. Differences in dose rates (electron beam versus gamma versus x-ray) can affect chemical properties and thus sensory qualities of irradiated almonds. Dose rate affects chemical reactions following second order (and higher) kinetics, such as radical recombination (FAO/IAEA/WHO 1999). Thus, radiolytic products can be influenced by the type of irradiation used—gamma, x-ray, or electron beam.The minimum dose level that will affect sensory quality must be ascertained. Practical considerations include availability of equipment and facilities that can specifically handle nuts. Cost of irradiation treatment, labeling requirements, regulations in countries to which nuts are exported, and consumer acceptance are also important considerations. References Aegerter A, Folwell R. 2001. Selected alternatives to methyl bromide in the postharvest and quarantine treatment of almonds: an economic perspective. J Food Process Preserv 25(6):389–410. Ahmed M. 2001. Disinfestation of stored grains, pulses, dried fruits and nuts, and other dried foods. In: Molins RA, ed. Food Irradiation: Principles and Applications. New York, NY: John Wiley and Sons, p. 77–112. Ahn D. 2002. Production of volatiles from amino acids homopolymers by irradiation. J Food Sci 67(7):2565–2570. Ahn D, Jo C, Olson DG. 2000.Analysis of volatile components and the sensory characteristics of irradiated raw pork. Meat Sci 54(2):209–215. Almond Board of California (U.S.). 2004 September 06.ABC Action Plan Update. Modesto, CA: Almond Board of California. Issue nr: 4. 7 p. Available from: Almond Board of California Modesto, CA. Almond Board of California (U.S.). 1998. Guide to California almonds. Modesto, CA:Almond Board of California. Brochure nr:VP 9/98. 6 p.Available from:Almond Board of California Modesto, CA. Aziz N, Moussa L. 2004. Reduction of fungi and mycotoxins formation in seeds by gammaradiation. J Food Safety 24:109–127. Braddock J, Sims C, O’Keefe S. 1995. Flavor and oxidative stability of roasted high oleic acid peanuts. J Food Sci 60(3):489–493. California Pistachio Commission (U.S.). 2005. Homegrown. Fresno, Calif: California Pistachio Commission.Available from: www.pistachios.org.Accessed February 05 2005.

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Isaacs S,Aramini J, Ciebin B, Farrar J,Ahmed R, Middleton D, Chandran AU, Harris LJ, Howes M, Chan E, Pichette SC, Campbell K, Gupta A, Lior LY, Pearce M, Clark C, Rodgers F, Jamieson F, Brophy I, Ellis A. 2005.An international outbreak of Salmonellosis associated with raw almonds contaminated with a rare phage of Salmonella Enteriditis. J Food Prot 68(1):191–198. Changa T, Matta F, Silva J. 1988. Pecan kernel quality as affected by antioxidant and irradiation. Proceedings of the annual convention—Southeastern Pecan Growers Association. 81:59–63. [CDC] Centers for Disease Control and Prevention—Department of Health and Human Services (U.S.). 2003 January. Update on Salmonella serotype Enteriditis infections, outbreaks and the importance for traceback and timely reporting of outbreaks. Atlanta, GA.: 9 p. Available from: CDC Division of Bacterial and Mycotic Diseases, Atlanta, Georgia. Chiou R, Lin C, Shyu S. 1990. Property characterization of peanut kernels subjected to gamma irradiation and its effect on the outgrowth and aflatoxin production by aspergillus parasiticus. J Food Sci 55(1):210–217. Curtis C, Sibbett G, Gerdts M, Clark J. 1983.Yield of subsequent crop when tree shaking is used to remove mummy almonds for navel orangeworm (Lepidoptera: Pyralidae). J Econ Entomol 76(3):632–633. [FDA] Food and Drug Administration. 2002. Hughson nut almonds from California recall update. Rockville, MD: Food and Drug Administration. Available from: http:// 209.58.136.120/reCAll/f/014/f45512.htm.Accessed 2002 October 1. [FDA-CFSAN] Food and Drug Administration—Center for Food Safety and Applied Nutrition. Foodborne Pathogenic Microorganisms and Natural Toxins Handbook. 1992. Jan 04. Aflatoxins. Rockville, MD: FDA-CFSAN. Available from: www.cfsan.fda.gov/ ~mow/chap41.html.Accessed 2005 February 22. [FDA-HHS] Food and Drug Administration—Health and Human Services. Federal Register Online. 2001. May 10. Food irradiation coalition c/o national food processors association; filing of food additive petition; ammendment. Rockville, MD: FDA-HHS. Volume 66(91). P. 23943–23944. Available from: www.wais.access.gpo.gov. Accessed 2005 February 28. [FAO/IAEA/WHO] Food and Agricultural Organization of the United Nations/International Atomic Energy Agency and World Health Organization. 1999. Joint FAO/IAEA/WHO Study group on high dose irradiation (wholesomeness of food irradiated above 10 kGy) (1997: Geneva, Switzerland). WHO Technical Report Series. Nr. 890. World Health Organization 1999. Ingram M, Farkas J. 1976. Microbiology of food pasteurised by ionising radiation. Acta Alimentaria 6 (2) 123-185. International Tree Nut Council. 1998. Jan. Nuts and aflatoxins. Hamburg: The executive committee of the healthy nut initiative. 25 p.Available from: Healthy Nut Initiative, c/o ipr,idée public relations, Spandenteich 1, 20099 Hamburg. www.treenuts.org. Jo C and Ahn DU. 2000.Volatiles and oxidative changes in irradiated pork sausage with different fatty acid composition and tocopherol content. J Food Sci 65(2):270–275. Johnson J and Vail P. 1989. Damage to raisins, almonds, and walnuts by irradiated Indian meal moth and navel orangeworm. J Econ Entomol 82(5):1391–1394. Johnson J and Vail P. 1987. Adult emergence and sterility of Indian meal moths (Lepidoptera: Pyralidae) irradiated as pupae in dried fruits and nuts. J Econ Entomol 80(2):497–501. Kader A,Thompson J. 2002. Postharvest handling systems: tree nuts. In: Kader AA, technical ed. Postharvest technology of horticultural crops, 3rd ed. Oakland, CA: University of California, p. 399–406.

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Kinderlerer J, Johnson S. 1992. Rancidity in hazelnuts due to volatile aliphatic aldehydes. J Sci Food Agric 58(1):89–93. King A, Miller M, Eldridge L. 1970. Almond harvesting and microbial flora. Appl Micro 20(2):208–214. Kiss, R. 2002. Time to consider. Blue Diamond Grower News [serial online]; July/August 2002:1–3. Available from: Blue Diamond Growers via the Internet. Accessed 2002, October 1. Kwakwa A. 2003. High-dose irradiation of almonds: a preliminary investigation into its effect on lipid peroxidation and rancidity [M.Sc thesis]. Orange, CA: Chapman University. 46 p.Available from: Food Science and Nutrition Department, Orange, CA. Matic S, Mihokovic V, Katusin-Razem B, Razem D. 1990.The eradication of Salmonella in egg powder by gamma irradiation. J Food Prot 53(2):111–114. Miyahara M, Saito A, Kamimura T, Nagasawa T, Ito H, Masatake T. 2002. Hydrocarbon productions in hexane solutions of fatty acid methyl esters irradiated with gamma rays. J Health Sci 48(5):418–426. Monk J, Beuchat L, Doyle M. 1995. Irradiation inactivation of food-borne microorganisms. J Food Prot 58(2):197–208. Nam K,Ahn D. 2003. Combination of aerobic and vacuum packaging to control lipid oxidation and off-odor volatiles of irradiated raw turkey breast. Meat Sci 63(3):389–395. Narvaiz P, Lescano G, Kairiyama E. 1992. Irradiation of almonds and cashew nuts. Food Sci Technol 25(3):232–235. Nawar W. 1978. Reaction mechanisms in the radiolysis of fats: a review. J Agric Food Chem 26(1):21–25. Nawar W. 1977. Radiation chemistry of lipids. In: Elias PS, Cohen AJ, eds. Radiation chemistry of major food components.Amsterdam: Elsevier Scientific, p. 21–61. Newsome R. 1987. Perspective on food irradiation. Food Technol 41(2):100–101. Niemira B, Sommers CH, Boyd G. 2001. Irradiation inactivation of four Salmonella serotypes in orange juices with various turbidities. J Food Prot 64(5):614–617. O’Mahony M, Wong S, Odbert N. 1985. An initial sensory examination of the effect of postharvest irradiation on almonds. J Indust Irrad Tech 3(2):135–140. Rajkowski K,Thayer D. 2000. Reduction of Salmonella spp. and strains of Escherichia coli O157:H7 by gamma irradiation of inoculated sprouts. J Food Prot 63(7):871–875. Sang S, Lapsley K, Jeong W-S, Lachance P, Ho C-T, Rosen R. 2002. Antioxidative phenolic compounds isolated from almond skins (Prunus amygdalus batsch). J Agric Food Chem 50(8):2459–2463. Santos G. 2001.The effects of low-dose irradiation on lipid oxidation in almonds (Prunus amydalus) [M.Sc thesis]. Orange, CA: Chapman University. 43 p. Available from: Food Science and Nutrition Department, Orange, CA. Sattar A, Jan M,Ahmad A,Wahid M, Khan I. 1989. Irradiation disinfestation and biochemical quality of dry nuts.Acta Alimentaria 18(1):45–52. Shahidi F, Pegg R B. 1994. Hexanal as an indicator of the flavor deterioration of meat and meat products. In: Ho C-T, Hartman TG, Eds. Lipids in food flavors. ACS Sym Ser 558. Washington, D.C., U.S.A.:Am Chem Soc, p. 256–279. Souza C. 2002.Almond industry promotes safety in food and on the farm.AG Alert [serial online], September 11, 2002.Available from: California Farm Bureau Federation via the Internet.Accessed 2003 April 05. Spoto MHF, Domarco RE,Walder JMM, Scarminio IS, Bruns RE. 1997. Sensory evaluation of orange juice concentrate as affected by irradiation and storage. J Food Process Preser 21(2):179–191.

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Temcharoen P,Thilly WG. 1982. Removal of aflatoxin B1 toxicity but not mutagenicity by 1 megarad gamma radiation of peanut meal. J Food Safety 4:199–205. Thayer DW, Rajkowski KT, Boyd G, Cooke PH, Soroka DS. 2003. Inactivation of Escherichia E. coli O157:H7 and Salmonella by gamma irradiation of alfalfa seed intended for production of food sprouts. J Food Prot 66:175–181. Thomas P. 1988. Radiation preservation of foods of plant origin. Part VI. Mushrooms, tomatoes, minor fruits and vegetables, dried fruits, and nuts. CRC Crit Rev Food Sci Nutr 26(4):313–358. [USDA] United States Department of Agriculture. 1984. Composition of foods: nuts and seed products. Raw, processed, prepared.Agricultural Handbook nr. 8–12.Washington, D.C., MD, U.S.A.: Government Printing Office. [USDA] United States Department of Agriculture. 2002. Rules and Regulations. Federal Register. Federal Register 67(205):65016–65029. [USDA-AMS] United States Department of Agriculture—Agricultural Marketing ServiceFruit and Vegetable Programs-Fresh Products Branch. 2003a Sept. U.S. Standards of Pistachio Nuts in the Shell. Washington, D.C., MD, U.S.A. Available from: www.ams.usda.gov. [USDA-AMS] United States Department of Agriculture—Agricultural Marketing ServiceFruit and Vegetable Programs-Fresh Products Branch. 2003b Sept. U.S. Standards of Shelled Pistachio Nuts.Washington, D.C., MD, U.S.A.Available from: www.ams.usda.gov. [USDA-HTP] United States Department of Agriculture—Horticultural and Tropical Products Division—Foreign Agricultural Service. 2004. Horticultural and tropical products 2004 reference guide.Washington, D.C., MD, U.S.A.Available from: www.fas.usda.gov/htp. University of California and Almond Board of California (U.S.). 2001 September. Producing quality almonds: food safety starts on the farm. 114171 Almond brochure. 6 p.Available from:Almond Board of California, Modesto, CA. University of California at Davis. 2005. UC Pest Management Guidelines-Pests of Almond. Davis, CA: University of California Statewide Integrated pest management program. Available from: www.ipm.ucdavis.edu/PMG/selectnewpest.almonds.html. Accessed 2005 April 08, 2005. Urbain W M. 1977. Radiation chemistry of proteins. In: Elias P S, Cohen AJ, eds. Radiation chemistry of major food components.Amsterdam:Elsevier Scientific, p. 63–130. Uthman RS, Toma RB, Garcia R, Medora NP, Cunningham S. 1998. Lipid analyses of fumigated vs. irradiated raw and roasted almonds. J Sci Food Agric 78(2):261–266. Wilson GY. 1990.The effectiveness of gamma processing as compared to propylene oxide for controlling mold on English walnuts (juglans regia). Orange, CA: Chapman University, 28 p.Available from: Food Science and Nutrition Department, Orange, CA. Zalom FG, Bentley WJ. 1985. Southern fire ant (Hymenoptera: Formicidae) damage to harvested almonds in California. J Econ Entomol 78(2):339–341.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 14 IRRADIATED GROUND BEEF FOR THE NATIONAL SCHOOL LUNCH PROGRAM Xuetong Fan

Introduction This chapter provides background information on the introduction of irradiated ground beef into the National School Lunch Program, and reviews the importance of providing safe foods in schools, the specifications of irradiated ground beef, and the sensory attributes of irradiated beef supplied to the National School Lunch Program. Original research on sensory evaluation of irradiated ground beef after 12 months of storage at ⫺18° C is also reported. More than 36 million children receive meals daily (year 2003) in the nation’s public schools and many private schools through the federally funded National School Lunch Program and School Breakfast Program (FNS 2004). The purposes of the programs are to provide nutritionally balanced low-cost or free meals to children and to help support the agricultural economy.The federal cost of school meal programs was 8.8 billion dollars in fiscal year 2003. Several USDA agencies cooperate in the purchasing and distributing of commodity foods through the National School Lunch Program.The USDA Agricultural Marketing Service (AMS) and the Farm Service Agency (FSA) are responsible for purchasing commodities. The USDA Food and Nutrition Service (FNS) administers the program at the federal level. At the state level, the programs are usually administered by the State Department of Education or Agriculture, which operates the programs through agreements with school food authorities. Schools that choose to participate get cash subsidies and donated commodities from the USDA for each meal served.

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Table 14.1. Number of Illnesses Associated with Reported Foodborne Outbreaks Resulting from Foods Prepared in Restaurants, Private Homes, Schools, and Other Locations, 1973–1999 Location of Food Preparation Restaurant Private home School Other Unknown Total

Outbreaks

Illnesses

Illnesses per Outbreak

8,465 2,404 547 3,704 711 15,831

148,548 30,198 46,461 207,191 15,085 447,483

17.5 12.6 84.9 55.9 21.2 28.3

Percentage of Outbreaks with 50+ Illnesses 7.3 3.8 50.5 25.0 9.8 12.5

Sources: General Accounting Office (GAO). 2003. School meal programs: Few instances of foodborne outbreaks reported, and opportunities exist to enhance outbreak data and food safety practices. GAO-03-530. Available from U.S. General Accounting Office,Washington D.C.

Foodborne Illnesses in School Providing safe foods to children is important because children’s immune systems are not fully developed, placing them at a higher risk of complications from some foodborne illness, such as Escherichia coli O157:H7 and Salmonella.The infection rate for E. coli O157:H7 is 8.2 per 100,000 children between 1 and 9 years old, the highest infection rate for any age group (Buzby 2001). Food safety is also important because the number of illnesses per outbreak in schools is higher than those that occurred in other food service locations (Table 14.1, GAO 2003).The total number of outbreaks in schools was low compared to other food service locations, accounting for about 3.5% of total outbreaks during the period of 1973–1999. However, these outbreaks are responsible for about 10% of all outbreak-related illnesses during the period. The number of illnesses per outbreak at schools was the highest (84.9 illnesses/outbreak), and half of those outbreaks involved more than 50 students and/or teachers. To improve the safety of school meals, Congress asked the U.S. General Accounting Office (GAO) to determine the frequency and causes of reported foodborne illness outbreaks associated with federal school meal programs and to identify practices that can be used by federal, state, and local governments as well as other food providers to safeguard school meals. To find the causes of major outbreaks, GAO surveyed the state health officials in states where major outbreaks in schools occurred during the period of 1990–1999 (GAO 2003). During the 10-year period, 195 outbreaks occurred in schools, and 59 outbreaks involved 50 or more in-

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239

dividuals.Among the 59 outbreaks, 40 foodborne illness outbreaks were caused by school meals. Others were caused by foods brought from home, or they occurred at special events.The survey conducted by GAO on major outbreaks indicated that Norwalk-like viruses (eight out of 40) and Staphylococcus aureus (seven out of 40) were the most frequently reported causes of illness. Other causes of illnesses included: Salmonella (five out of 40) and Clostridium perfringens (four out of 40). Shigella (two out of 40), hepatitis A (two of 40), and Bacillus cereus (one out of 40) also caused illnesses in schools, although in lower frequency. In most of the remaining outbreaks, the agent that caused foodborne illness was never identified. Analysis of data from the Centers for Disease Control and Prevention (CDC) from 1973–1997 indicated that an etiology was not determined in 60% of reported outbreaks, and a specific food vehicle of transmission was not determined in 45% of outbreaks (Daniels and others 2002). For the period of 1973–1997, Salmonella was the most commonly identified pathogen, accounting for 36% of outbreak reports with a known etiology. The most frequently implicated vehicles are foods containing poultry (18.6%), salads (6.0%), Mexican-style food (6.0%), beef (5.7%), and dairy products (5.0%). For example, in 1998, 11 children were infected by E. coli O157:H7 in contaminated ground beef served in a taco meal in a Washington State school.Three of the children developed kidney failure (hemolytic uremic syndrome). Many of the outbreaks in schools are due to poor hygiene of food workers and improper food handling (GAO 2003).About half of 40 (19 of 40) major outbreaks associated with school meals were the result of poor food preparation and handling practices, and about six of the 40 outbreaks were due to foods that were contaminated before delivery to the school.After analysis of CDC’s foodborne outbreak database, a survey of state health officials, and consultation with food safety experts, GAO recommended USDA and schools to train and certify school food service workers, to use risk-based food safety procedures based on the Hazard Analysis and Critical Control Point (HACCP) system, to apply stringent purchasing specifications, and to purchase precooked and irradiated meat and poultry products.

Regulatory Allowance and Specifications of Irradiated Foods for Schools One of the provisions (Use of Approved Food Safety Technology) in the Farm Bill (Farm Security and Rural Investment Act of 2002 [HR 2646]),

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Section 4201(l), directs USDA to allow the use of any food safety technology approved by USDA or the Department of Health and Human Services, including irradiation, in the commodity purchase programs, including the National School Lunch Program (USC 2002). In addition, Congress amended the Richard B. Russell National School Lunch Act to address irradiated food products (USC 2004a).The amendment states that “The (USDA) Secretary shall develop policy and establish procedures for the purchase and distribution of irradiated food products in school meals programs” (USC 2004a,b). Further, it requested that “irradiated food products are available only at the request of States and school food authorities.” Other rules such as labeling, freedom of choice, and development of education programs on irradiation were also specified. The safety of irradiated foods has been extensively studied in the last half century.Thayer (2004) indicated that most of the studies conducted in animals and humans suggested that irradiated foods are safe, and consumption of the irradiated foods did not cause mutagenic or carcinogenic, or toxic effects.A detailed review on the safety of irradiated foods can be found in the Chapter 4 of this book. Irradiated foods are being carried by many supermarkets and restaurants and through mail orders, and are endorsed by many scientific organizations and industries, such as American Dietetic Association, American Medical Association, CDC, and World Health Organization (Osterholm and Norgan 2004). Despite these facts, there are many concerns about the safety and quality of irradiated foods. In November 2002, USDA requested public comments on implementing irradiated ground foods in the National School Lunch Program. The major comments against irradiation were as follows: Irradiated foods have not been proven safe and there is a lack of long-term health studies; irradiation induced toxic chemicals such as 2-dodecylcyclobutane; irradiation degraded nutritional content; irradiation masked the problems in the meat industry; and irradiation changed the flavor, odor, and texture of foods. Entities such as Public Citizen oppose serving irradiated foods to children, citing lack of studies on long-term health effects of irradiated foods (Public Citizen 2005). In May of 2003, AMS published the specifications for the purchase of irradiated ground beef in the National School Lunch Program (AMS 2003).According to AMS specifications, all ground beef will have a target average fat level of 15 ± 3% except for ground beef patties, which will not exceed 10% fat. The patty should weigh 3.0 ± 0.1 oz with thickness of 5/16 inch. Irradiated ground beef can be either in 10-lb frozen chubs or as individual quick-frozen patties. Either product must be packaged in FDA-approved packaging materials. The radiation source was not specified by AMS; therefore, all three types of irradiation (gamma, electron

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beam, and X-ray) can be applied. Because electron beam processing has limited penetration ability, to maintain dose uniformity in the packages, the size and dimension of the containers are defined. The maximum weight of ground beef in single containers is 20 lb.The depth of the container must not exceed 4.0 inches, the width must not exceed 14 inches, and the length must not exceed 20 inches.The containers must bear the required FSIS markings (Radura) for irradiated products and a “best if used by date”(180 days from date of production). Products must be packaged, placed into shipping containers, and frozen to 0°F (⫺18°C) within 72 hours from the time of their completion in the production lot. Products must be held in a frozen state throughout shipping, the irradiation process, and storage. Ground beef must be subjected to ionizing radiation to receive a dosage that is no less than 1.35 kGy and no more than 3.0 kGy; proper dosimetry has to be performed. Irradiated ground beef shall be tested for standard plate count, total coli forms, E. coli, and coagulate positive Staphylococci after final grinding and before freezing, and shall be tested for Salmonella and E. coli O157:H7 after completion of the irradiated process.

Sensory Properties of Irradiated Ground Beef One of the concerns of irradiated ground beef received by AMS and FNS was the possible change in sensory attributes such as flavor, odor, and texture. There have been several studies on effective tests of irradiation of ground beef in recent years (Table 14.2). Luchsinger and others (1997) irradiated (2.0 and 3.5 kGy) frozen ground beef (10 and 22% fat) and stored the samples for 14 days at ⫺19°C. Using a highly trained panel, researchers found that irradiation had minimal effects on flavor, texture, or aroma of ground beef patties.Wheeler and others (1999), using a trained panel, evaluated ground beef (19% fat) after 27–29 days of storage at ⫺28°C and found that irradiated (3 and 4.5 kGy) ground beef had less beef flavor and aroma and more off-flavor than the nonirradiated samples. Lopez-Gonzalez and others (2000), also using a trained panel, found that irradiated (2 kGy) fresh ground beef (20% fat) had less cooked beef/brothy flavor than the nonirradiated ones. There were no differences in other sensory attributes between irradiated and nonirradiated samples. There have also been studies using untrained panels or slightly trained panels. Murano and others (1998) irradiated and stored frozen ground beef patties (20% fat) in different packaging schemes for up to seven days at ⫺25°C. Researchers found that packaging type and storage affected

242

ND: not defined.

Lopez-Gonzalez and others 2000 Giroux and others 2001 Vickers and Wang 2002 Lorenzen and Heymann 2003 Fan and others 2004

20

23

ND

ND

15

Aerobic

Air

Vacuum

Vacuum

Vacuum

Vacuum/ 11, 22 aerobic Vacuum/ 20 aerobic Vacuum 19

Fat Type of Level Packaging (%)

1.35, 3, gamma

1.0 kGy, e-beam

1.5, e-beam

0.5–4, gamma

Frozen

Frozen

Fresh

Fresh

Fresh

Consumer

Consumer

Consumer

Non-trained

Trained

62–104d, ⫺28°C

Consumer 2, both e-beam and gamma

27–29d, ⫺28°C

Frozen

3, 4.5, gamma

180d, frozen

ND, frozen

3–4d, ND

7d, 4°C

1–2d, 5°C

7d, ⫺25°C

Slightly trained Trained

⫺3°C

2.0, e-beam

14d, ⫺19°C

Storage Time and Temperature

Trained

Type of Panel

Frozen

Status of Samples during Irradiation

2.0/3.5, x-ray

Dose (kGy), Type of Irradiation

A Summary of Recent Studies on Sensory Evaluation of Irradiated Ground Beef

Luchsinger and others 1997 Murano and others 1998 Wheeler and others 1999

Researchers

Table 14.2.

No effect

Little effect

Juicier

No effect (taste or odor)

Minimal effect on flavor, texture, or aroma Lower aftertaste when packed aerobically Trained (less beef flavor, aroma; more off-flavor); Consumer (less taste score, 4.5 kGy) Less cooked beef/brothy flavor

Effect of Irradiation

Irradiated Ground Beef for the National School Lunch Program

243

texture and aftertaste of irradiated ground beef, but no undesirable change in flavor, texture, juiciness, or aftertaste was caused by irradiation. Ground beef patties irradiated under vacuum and stored in air were more tender than the nonirradiated samples.Wheeler and others (1999) evaluated ground beef after 62–104 days of storage at ⫺28° C. A consumer panel found that patties irradiated with 4.5 kGy had less taste than the nonirradiated patties whereas no difference was found in lower doses. Giroux and others (2001), using an untrained panel, found no significant difference in odor and taste between irradiated (up to 4 kGy) and nonirradiated ground beef patties (23% fat) during seven days of storage at 4° C.Vickers and Wang (2002), using an untrained panel, found that ratings of overall liking, flavor liking, and texture liking for irradiated (1.5 kGy) fresh ground beef (fat content not defined) did not differ from those of the nonirradiated patties.The rating of juiciness was higher in irradiated patties than the nonirradiated ones. Lorenzen and Heymann (2003), using a consumer panel, found that irradiation of frozen ground patties (fat content not defined) at 1.0 kGy had little effect on overall liking, tenderness, juiciness, and flavor of cooked patties. From the literature, we can conclude that trained panels, in some cases, noted that irradiated ground beef at doses above 2 kGy had more undesirable sensory properties than nonirradiated beef. Consumer panels or untrained panels generally found minimal differences in sensory attributes between patties irradiated in low doses (less than 3.0 kGy) and nonirradiated ones. In a difference test using a consumer panel, Zienkewicz and Penner (2004) irradiated ground beef (25% fat) at a dose of 1.5 kGy, and the panel could not differentiate between the two types of ground beef. For both the initial and the three-month sensory tests, irradiated and nonirradiated ground beef were judged to be the same in terms of sensory attributes. None of the research cited has studied ground beef with the specifications developed by AMS, such as fat level of 15% and storage time of 180 days. In most of the research cited, patties were irradiated and stored fresh, which differs from AMS specification for frozen ground beef.To address the concerns about the palatability of irradiated ground beef, Fan and others (2004), using untrained panels, conducted a study to evaluate (1) the effects of irradiation (1.35 and 3.0 kGy) on the sensory properties of ground beef (15% fat) destined for the National School Lunch Program and (2) the sensory quality of irradiated ground beef after six months of storage.As a follow-up study, sensory evaluation was also conducted after 12 months, and the results are reported here. At 0, 6, and 12 months of storage at ⫺18° C after irradiation, ground beef patties were cooked from frozen state to an internal temperature of 80° C using convection ovens. Aroma, taste, texture, aftertaste, and overall degree of liking of the cooked

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patties were rated on a 9-point fully labeled category scale (1 = dislike extremely to 9 = like extremely). The degree of liking of any sensory attribute between nonirradiated samples and the two irradiated samples was similar for 0, 6, or 12 months of storage (Table 14.3). Furthermore, there was no significant (P>0.05) difference in the degree of liking of any sensory attribute between the two irradiated samples (that is, 1.35 kGy vs. 3.0 kGy) for any storage period.The average ratings of liking for most of the sensory attributes were between 5 (neither like nor dislike) and 6 (like slightly). However, storage had a significant effect on the ratings for aroma, taste, aftertaste, and overall liking. In general, the ratings for the above sensory attributes were significantly (P<0.05) higher at six months than those at zero month, and the ratings for aroma, taste, and overall liking were higher at 12 months than at zero month. No change was found in texture during storage. No change was found in any of the sensory attributes between six and 12 months. The increased ratings on some of the attributes during storage Table 14.3. Effect of Irradiation and Storage on the Degree of Likingx of Ground Beef Patties Irradiated at 0, 1.35, and 3 kGy at 0, 6, and 12 Months of Storage at ⫺18°C Dose (kGy)

Aroma

Taste

Texture

Aftertaste

Overall 5.5±1.7 bc 5.6±1.7 abc 5.4±1.7 c

0 1.35 3.0

5.3±1.6 bcdy 5.3±1.6 cd 5.2±1.7 d

0 month (n=130) 5.6±1.7 bc 5.5±1.7 a 5.8±1.8 abc 5.3±1.8 a 5.6±1.7 c 5.2±1.8 a

5.4±1.6 bc 5.4±1.6 bc 5.3±1.6 c

0 1.35 3.0

5.6±1.5 abc 5.7±1.4 a 5.5±1.6 abcd

6 months (n=124) 5.9±1.7 abc 5.5±1.6 a 6.1±1.5 a 5.6±1.5 a 6.1±1.8 a 5.3±1.6 a

5.7±1.5 ab 5.8±1.6 abc 5.8±1.5 a 6.0±1.5 a 5.6±1.6 abc 5.9±1.5 ab

12 months (n=112) 5.8±1.6 abc 5.3±1.6 a 6.0±2.3 ab 5.6±1.6 a 6.0±1.7 abc 5.5±1.8 a 0.4 0.4 * NS

5.4±1.6 abc 5.6±1.5 abc 5.6±1.5 abc 6.0±1.3 a 5.5±1.6 abc 5.8±1.6 abc 0.4 0.4 * *

0 5.7±1.4 a 1.35 5.7±1.4 a 3.0 5.7±1.6 ab LSD 0.4 Overall storage *z effect

Sources: Data on 0 and 6 months are adapted from Fan and others (2004). Sensory evaluation of irradiated ground beef for the National School Lunch Program. Journal of Food Science 69:S394-S3*7. x Liking scores are 9-point fully labeled category scales where 1 = dislike extremely and 9 = like extremely. y Means with the same letters are not significant difference (LSD, P>0.05). z * and NS indicate the overall significant (P<0.05) or non-significant effect of storage time, respectively.

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Table 14.4. Effect of Irradiation and Storage on the Degree of Likingx of Ground Beef Patties Rated by the 36 Teenage Panelists at 0 and 12 Months of Storage at ⫺18° C Dose (kGy)

Aroma

Taste

Texture

Aftertaste

Overall

0 1.35 3.0

5.3±1.6 ay 5.3±1.6 a 5.2±1.7 a

0 month (n=24) 5.6±1.7 a 5.5±1.7 a 5.8±1.8 a 5.3±1.8 ab 5.6±1.7 a 5.2±1.8 ab

5.4±1.6 a 5.4±1.6 a 5.3±1.6 a

5.5±1.7 a 5.6±1.7 a 5.4±1.7 a

0 1.35 3.0

6.0±0.6 a 5.8±1.3 a 5.7±1.7 a

12 months (n=12) 5.0±2.1 a 4.5±1.6 abc 5.0±1.7 a 5.8±1.2 a 4.3±1.8 bc 4.8±1.9 a 5.6±1.8 a 3.8±2.2 c 4.2±2.0 a

5.1±1.4 a 5.3±1.2 a 5.0±1.6 a

Sources: Data on 0 month are adapted from Fan X. and others (2004). Sensory evaluation of irradiated ground beef for the National School Lunch Program. Journal of Food Science 69:S394–S387. x Liking scores are 9-point fully labeled category scales where 1= dislike extremely and 9 = like extremely. y Means with the same letters are not a significant difference (LSD, P>0)

may be due to the reduction of some undesirable properties of irradiated samples during storage. Mattison and others (1986) reported similar results that sensory attributes of irradiated pork loins improved during storages. Some of the panelists who participated in the studies at zero and 12 months were younger than 20 years of age. The ratings of aroma, taste, texture, aftertaste, and overall degree of liking given by teenage panelists were similar for irradiated and nonirradiated ground beef at either zero or 12 months although the ratings of texture were lower at 12 months than at zero month (Table 14.4). Furthermore, there was no difference in the average ratings of any attribute between the panelists younger than 20 years of age and the rest of the panelists. A triangle test conducted on zero month ground beef also indicated that the difference between irradiated and nonirradiated ground beef was so minimal that consumers were unlikely to distinguish irradiated ground beef from the nonirradiated products (Fan and others 2004). Although irradiated ground beef has been available to schools since September of 2004, and school districts from several states initially ordered irradiated ground beef, the orders were eventually canceled, mainly due to the higher cost of the meat.The irradiated ground beef was 20–75 cents more per pound than nonirradiated ground beef (Watkins 2004). The price will most likely go down if more products are ordered. Despite the efforts by FNS and other agencies on consumer education through school food service meetings, brochure distribution to schools,

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publishing information about food irradiation on Web sites, and so on, there are still concerns about the safety and sensory properties of irradiated ground beef on the part of parents and schools. Continuing the education programs will definitely help consumers’ awareness of irradiated ground beef in schools, which could lower the incidence of foodborne illness. Studies have found that consumers not receiving education were skeptical and had more negative perceptions about irradiation technology (Vickers and Wang 2002; Zienkewicz and Penner 2004). Educating consumers on irradiation technology had the most significant impact on their perceptions of food irradiation.

Conclusion Providing safe food to schoolchildren is very important because children are at high risk for complications from some foodborne illnesses.The potential for a number of illnesses in an outbreak is high because children are grouped together at school during mealtimes and often eat the same meals.To improve food safety in schools, purchasing and distributing irradiated food products, such as ground beef, has been recommended and required by law to be offered to schools through the National School Lunch Program. USDA, AMS has published the procurement specifications for the purchase of irradiated ground beef. However, some concerns exist about the sensory attributes of irradiated ground beef. Studies have been conducted to evaluate the sensory attributes of irradiated ground beef during 12 months of storage at ⫺18° C. Results demonstrate that irradiation at doses of 1.35 and 3.0 kGy, as specified by AMS, did not have significant influence on the ratings for aroma, texture, taste, aftertaste, and overall degree of liking of ground beef evaluated either immediately after irradiation or after six and 12 months of storage at ⫺18° C.The successful implementation of irradiated ground beef in schools will depend on consumer (parents and schools) education efforts about the safety of irradiation technology and sensory quality of irradiated foods and on finding ways to reduce the cost of irradiated foods.

Acknowledgements The author thanks Kimberly J. B. Sokorai, Robert Richardson and Glenn Boyd for technical assistance, and Diane VanHekken, Brenda Halbrook, and Margaret Venuto for reviewing the manuscript.

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References AMS (Agriculture Marketing Service). 2003.Technical requirements schedule (GB-2003) for ground beef items, frozen. Available from USDA, AMS, Livestock and Seed Program, Washington D.C. http://www.ams.usda.gov/lscp/beef/TRS-%20GB-%202003%20%200529-03.pdf.Accessed January 25, 2005. Buzby JC. 2001. Children and microbial foodborne illness. Food Review 24(2):32–37. Daniels NA, Mackinnon L, Rowe SM, Bean NH, Griffin PM, Mead PS. 2002. Foodborne disease outbreaks in United States Schools. Pediat Infect Dis J 21:623–628. Fan X, Niemira BA, Rajkowski KT, Phillips J, Sommers CH. 2004. Sensory evaluation of irradiated ground beef for the National School Lunch Program. J Food Sci 69:S394–S3*7. FNS (Food Nutrition Service), USDA. 2004. Program data, National School Lunch Program. http://www.fns.usda.gov/pd/slmain.htm.Accessed January 25, 2005. GAO (General Accounting Office). 2003. School meal programs: Few instances of foodborne outbreaks reported, and opportunities exist to enhance outbreak data and food safety practices. GAO-03-530. Available from U.S. General Accounting Office, Washington D.C. http://www.gao.gov/new.items/d03530.pdf. Accessed January 25, 2005. Giroux M, Ouattara B,Yefsah R, Smoragiewicz W, Saucier L, Lacroix M. 2001. Combined effects of ascorbate acid and gamma irradiation on microbial and sensorial characteristics of beef patties during refrigerated storage. J Agric Food Chem 49:919–925. Lopez-Gonzalez V, Murano PS, Brennan RE, Murano EA. 2000. Sensory evaluation of ground beef patties irradiated by gamma rays versus electron beam under various packaging conditions. J Food Qual 23:195–204. Lorenzen CL, Heymann H. 2003. Effect of irradiation on consumer perception and descriptive analysis of ground beef patties. J Mus Food 14(3):233–239. Luchsinger SE, Kropf DH, Chambers IVE, Garcia Zepeda CM, Hunt MC, Stroda SL, Hollingsworth ME, Marsden JL, Kastner CL. 1997. Sensory analysis of irradiated ground beef patties and whole muscle beef. J Sens Study 12:105–126. Mattison ML, Kraft AA, Olsen DG,Walker HW, Rust RE, James DB. 1986. Effect of low dose irradiation of pork loins on the microflora, sensory characteristics and fat stability. J Food Sci 51:284–287. Murano PS, Murano EA, Olson DG. 1998. Irradiated ground beef: sensory and quality changes during storage under various packaging conditions. J Food Sci 63:548–551. Osterholm MT, Norgan AP. 2004.The role of irradiation in food safety. New England J Med 350:1898–1901. Public Citizen. 2005. Irradiated food in school lunches. Public Citizen, Washington, D.C. Also available at http://www.citizen.org/cmep/foodsafety/food_irrad/schoollunch. Accessed March 28, 2005. Thayer DW. 2004. Irradiation of food—helping to ensure food safety. New England J Med 350:1811–1812. USC (U.S. Congress). 2002. Farm Security and Rural Investment Act of 2002. Public Law 107-171, May 13, 2002. Sec 4202. USC (U.S. Congress). 2004a.Amendments to Richard B. Russell National School Lunch Act. Public Law 108-265, June 30, 2004. Available at http://thomas.loc.gov/cgi-bin/cpquery/T?&report=hr445&dbname=cp108&.Accessed January 25, 2005. USC (U.S. Congress). 2004b. Child Nutrition Improvement and Integrity Act. Available at http://thomas.loc.gov/cgi-bin/cpquery/T?&report=hr445&dbname=cp108&. Accessed January 25, 2005.

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Vickers ZM,Wang J. 2002. Liking of ground beef patties is not affected by irradiation. J Food Sci 67:380–383. Watkins C. 2004. Irradiate the food supply. Inform 15(12):758–759. Wheeler T, Shackelford S, Koohmaraie M. 1999.Trained sensory panel and consumer evaluation of the effects of gamma irradiation on palatability of vacuum packaged frozen ground beef patties. J Anim Sci 77:3219–3244. Zienkewicz LSH, Penner KP. 2004.Consumer’s perceptions of irradiated ground beef after education and product exposure. Food Protect Trends 24(10):740–745.

Disclaimer Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 15 POTENTIAL APPLICATIONS OF IONIZING RADIATION Myung-Woo Byun, Cheorun Jo, and Ju-Woon Lee

Introduction Food irradiation is known to be the best method for controlling pathogenic microorganisms and one of the best alternatives to the chemical fumigants or preservatives usually used for a sanitation treatment for international trade (WHO 1999). Irradiation technology has been officially adopted by international organizations (WHO/IAEA/FAO) and experts (WHO 1999) due to effectiveness in food, wholesomeness, and economic benefits. Besides the sanitary purposes, irradiation has been studied to reduce or eliminate undesirable or toxic materials including food allergens (Lee and others 2000; Lee and others 2001b), carcinogenic volatile N-nitrosamines (Ahn and others 2002a), biogenic amines (Kim and others 2003), embryotoxicity of gossypol (Jo and others 2003c), and phytic acid with enhancement of the antioxidant activity (Ahn and others 2004). In addition, irradiation has been shown to enhance color of low-nitrite meat products (Byun and others 1999) and low-salt fermented foods (Byun and others 2000b; Lee and others 2002). On the other hand, Byun and others (2002b) observed the breakdown of chlorophyll by irradiation, which can be used in oil processing. Based on this result, an application for color removal of green tea leaf extract (Jo and others 2003a) was developed.The commercial application of irradiation for the color improvement of plant-derived products without changing their beneficial biological activities was adopted in foods and cosmetics (Jo and others 2003b; Byun and others 2004a). There is a great potential for an application of irradiation as a new processing technology such as the development of traditional fermented 249

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foods and the reduction of undesirable or toxic compounds by irradiation. In this chapter, some of the background research and the results of recent studies are introduced and discussed for potential future applications.

Reduction of Food Allergies by Ionizing Radiation Food allergies are an emerging public health problem, especially in developed countries (Besler and others 2001). Food allergies are most prevalent in young children, affecting as many as 8% of children younger than three years and approximately 1% to 2% of the general population, and they are increasing gradually (Besler and others 2001).The relatively high prevalence of food allergies in infants and toddlers is due to an immature gastrointestinal epithelial membrane barrier, which allows more proteins to move through the barrier and into the circulatory system. In general, allergens, specific proteins, have unique properties that are predominantly water-soluble, heat- and acid-stable, and relatively resistant to a proteolytic digestion. Their molecular weights are in the range of 15 to 60 kilodaltons (kDa) (Metchlfe and others 1997). Major allergenic foods are eggs, cow’s milk, fish, shrimp, peanuts, tree nuts, wheat, and others (Sampson 2004). Many studies have been conducted to reduce food allergies. Chemical reagents, enzymatic digestion, and physical treatments using heat or high pressure were undertaken to induce conformational changes of allergens (Besler and others 2001; Mine and others 2003; Olsen and others 2003). Among the approaches, only one method using proteolytic enzyme has been commercially applied to the hydrolyzed hypoallergenic formula of cow’s milk (Chandra 2002; Svenning and others 2000). Food irradiation technology has been applied to reduce food allergies (Byun and others 2000a; Lee and others 2001a). Irradiation of proteins produces a structural denaturation (Hates and others 1995), and creates changes in the binding ability of IgE against allergens.The IgE ELISA inhibition test indicated the IgE-binding capacities of irradiated-ovoalbumin and –ovomucoid were reduced to 1/80 and 1/20, respectively (Fig. 15.1) (Lee and others 2002). Model food allergens were monitored to examine the reduction of their allergenicity by an ionizing radiation. Because a clinically significant result on the reduction of the allergy was reported (Jeon and others 2002), it is expected that the research on the allergy reduction using irradiation technology will be accelerated. At present, the study for commercial application is being conducted (Seo and others 2004).

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Figure 15.1. Ovalbumin (OVA) IgE ELISA inhibition assay with Native- and IrradiatedOVA.The binding capacities of Irradiated-OVA were only 1/80 of the controls (50% inhibition concentration: OVA-0.1 μg/mL, Irradiated-OVA-8 μg/mL), respectively. (•, Native OVA; •, Irradiated-OVA; 䉲, ß-Lactoglobulin)

Volatile N-nitrosamine and Residual Nitrite Reduction Volatile N-nitrosamines (VNAs) are present in many foodstuffs (Zou and others 1994; Seel and others 1994), rubber products (Novitch 1983), and tobacco (Tricker and others 1989). Many VNAs are resistant to heat, but they can be cleaved photolytically by UV irradiation because of their chemical properties. Many studies have been performed to inhibit nitrosamine formation with dietary compounds such as ascorbic acid (Vermeer and others 1999), green tea (Yang and Wang 1993), and phenol compounds (Bartsch and others 1988). Wierbicki and Brynjolfsson (1979) reported earlier that irradiation ster-

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ilization with Co-60 and Cs-137 reduced nitrite and VNA levels in cured meat products.This research raised the possibility for reducing the nitrite and nitrosamines in a wide range of food systems. Since then, no research related to the effects of gamma irradiation on VNAs has been reported. Ahn and others (2002a) studied the breakdown of VNAs dissolved in distilled water, dichloromethane, or ethanol using a gas chromatograph coupled to a thermal energy analyzer. Results showed that solvents had an effect on the reduction of VNAs by gamma irradiation. Nitrosodimethylamine (NDMA) and nitrosopyrolidine (NPYR), when dissolved in distilled water, were most sensitive to irradiation breakdown; those dissolved in ethanol were most resistant to irradiation. All of the VNAs dissolved in three solvents were undetectable after irradiation of 5 kGy or above (Ahn and others 2002a).The authors concluded that presence of water is important for the breakdown of these compounds, similar to the hydrophotolysis of the nitrosamines by UV irradiation (Shuker and Tannenbaum 1983). The breakdown products from NDMA and NPYR by gamma rays did not recombine in vitro at pH 2, 3, and 4, but recombined in the presence of nitrite, indicating that gamma irradiation has a potential to be applied to real food systems without a reformation in the human stomach.Ahn and others (2002b) pointed out in a model sausage system study that the residual nitrite content was significantly reduced by gamma irradiation, and, in a vacuum state, the reduction was dose dependent. Table 15.1 shows that combination of gamma irradiation and vacuum packaging effectively reduced the residual nitrite level during storage.The packaging and irradiation effect was not shown in either NDMA or NPYR content immediately after irradiation. However, the contents of NDMA and NPYR increased during storage, and the difference was clearly shown by the treatments when compared with control (Table 15.2).Ahn and others (2003a) reported that the degradation rate of the sodium nitrite fitted a first-order model; a high linear correlation (R2 > 0.9) was observed and the degradation rate constant was 0.009 min⫺1. The radiolytic products of NDMA and NPYR dissolved in dichloromethane were identified by gas chromatography and mass spectrometry. The major radiolytic components of NDMA were ethyl acetate and 2-dimethyl propanol, and those of NPYR were 2butanone and 2-methyl-6-propylpiperidine (Ahn and others 2003a).

Biogenic Amines (BAs) Reduction Biogenic amines (BAs) are found in many kinds of fermented foods during aging, fermentation, and storage. BAs are formed by the action of mi-

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Table 15.1. Monitoring of Residual Nitrite Levels (ppm) of Sausage Prepared with 150 ppm Sodium Nitrite in Different Packaging and Irradiation Doses during Processing and Storage Storage Periods (Week)

Processingc 0

1

2

3

4

Irradiation Dose (kGy)

Packaging

Aerobic Vacuum SEMb Aerobic Vacuum SEMb Aerobic Vacuum SEMb Aerobic Vacuum SEMb Aerobic Vacuum SEMb

0

5

10

20

SEMa

122.7

122.7

122.7

122.7

1.98

81.2adxe 66.8ay 1.01 80.5a 74.8a 0.98 85.8a 79.3a 2.83 79.5a 66.7a 1.29 55.7ax 40.1ay 0.82

73.2ab 64.0a 1.76 73.4b 63.2ab 4.48 77.7bx 69.9by 0.88 73.7bx 54.5by 1.08 48.0bx 34.4aby 1.01

64.5bx 57.6by 0.64 65.5c 57.6b 3.34 71.8b 66.7b 1.43 65.2cx 47.4cy 0.60 44.3cx 32.2by 0.80

54.6c 45.6c 2.62 62.6dx 49.0by 0.60 62.1cx 49.0cy 1.95 57.4dx 41.5dy 0.54 39.2d 24.2c 2.53

2.25 0.79 0.69 3.97 1.67 2.12 1.08 1.46 0.85 1.91

a

Standard errors of the mean (n = 8). Standard errors of the mean (n = 4). c Nitrite level was analyzed immediately after emulsification. d Different letters (a–d) within a same row differ significantly (P<0.05). e Different letters (x,y) within a same column differ significantly (P<0.05). b

croorganisms through the decarboxylation of amino acids (Shalaby 1996; Silla Santos 1996). These basic nitrogenous compounds are known as toxic substances that cause diseases with food poisoning symptoms (Joosten 1988). BAs are also known as possible precursors of carcinogens, such as N-nitrosamines.They are frequently found in high concentrations in food, and their levels are not reduced by high-temperature treatment (Shalaby 1996; Silla Santos 1996). The effects of irradiation on nine BAs were studied (Kim and others 2004) and a significant degradation of putrescine, spermidine, and spermine was found when radiation doses were ⱖ 5 kGy.Various BAs can be formed in fermented soybean products by microorganisms during fermentation, and high levels of BAs were reported for soy products (Chin and Koehler 1983).The change in BAs levels depends on the amount of the soybean in the raw material, microbiological composition, duration of fermentation, and many other factors (Nout and others 1993).The initial

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Table 15.2. N-nitrosodimethylamine (NDMA) and N-nitrosopyrrolidine (NPYR) Levels (ppb) of Sausage Prepared with 150 ppm Sodium Nitrite in Different Packaging and Irradiation Doses during Storage Storage Periods (Week) 0

4

Irradiation Dose (kGy)

Packaging NDMA Aerobic Vacuum SEMb NPYR Aerobic Vacuum SEMb NDMA Aerobic Vacuum SEMb NPYR Aerobic Vacuum SEMb

0

5

10

20

SEMa

5.0 4.6 1.45

3.6 3.6 0.80

3.1 2.6 1.25

1.4 1.9 1.21

1.35 1.03

NDc ND -

ND ND -

ND ND -

0.78 0.53

16.4 11.6ad 9.60

11.1 11.2ab 7.92

7.9 5.2ab 6.74

4.7 NDb 3.33

8.91 2.83

24.9a 12.7a 3.50

3.3b 12.1a 2.94

NDb NDb —

2.81 2.22

2.9 1.6 1.14

NDb 3.1b 2.17

a

Standard errors of the mean (n = 8). Standard errors of the mean (n = 4). c Not detected. d Different letters (a, b) within a same row differ significantly (P<0.05). b

microbial population is an important factor influencing the formation of BAs, as suggested by Bover-Cid and others (2000). Kim and others (2003) hypothesized that irradiation can reduce BAs by decreasing the levels of microorganisms and investigated the hypothesis using Korean fermented soybean paste during fermentation at 25° C for 12 weeks.The authors detected putrescine, cadaverine, ß-phenylethylamine, spermindine, spermine, tryptamine, histamine, tyramine, and agmatine in the product. A significant difference was not observed in the BA contents between the control and irradiated samples immediately after gamma irradiation, but those of four BAs (putrescine, tryptamine, spermidine, and histamine) showed a significant reduction during the fermentation period.The authors indicated that gamma irradiation is an effective way to reduce some BAs amines detected in Korean fermented soybean paste by controlling the microorganisms during fermentation (Kim and others 2003).

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255

Reduction of Phytic Acid and Increase in Antioxidant Activity Phytic acid is widely found in cereals, nuts, legumes, oil seeds, pollen, and spores (Graf and Eaton 1990). Phytic acid [myoinositol hexaphosphate (IP6)] was historically considered to be an anti-nutrient. Structurally, phytic acid contains phosphorus, and it binds minerals such as calcium, iron, and zinc, causing a decrease of their bioavailability in human and animal models (Reddy and others 1989). However, phytic acid has been reported to be an antioxidant (Graf and Eaton 1990), anticarcinogenic (Shamsuddin and others 1997), and a hypoglycemic or hypolipidemic (Rickard and Thompson 1997). Phytic acid is considered to be an antioxidant agent because it is a potent inhibitor of the iron-catalyzed hydroxyl radical formation by chelating the free iron and then blocking the coordination site (Graf and Eaton 1990). In phytic acid-rich foods, trials for reducing phytic acid, including physical or chemical processing, genetic manipulation, or enzymatic hydrolysis, have been performed (Harland and Harland 1980; Siddhuraju and others 2002).Actually, some cereals including corn, barley, and rice mutants have been developed that contain significantly lower levels of phytic acid without reducing the total phophorus, and these should prove valuable for swine and poultry feed ingredients (Larson and others 2000). Additionally, Duodu and others (1999) reported that irradiation reduced phytic acid levels.These studies showed the possibility for reducing the phytic acid levels in foods. When phytic acid sodium salt dissolved in deionized distilled water was irradiated up to 20 kGy, a degradation of the phytic acid was clearly observed (Ahn and others 2003b). It was also found that the concentration of phytic acid had an effect on the degree of degradation.The radical scavenging activity using 1,1-diphenyl-2-picrylhydrazyl (DPPH) of phytic acid was significantly increased by irradiation (P<0.05) and was positively correlated with the irradiation dose.Ahn and others (2003b) used a lipid model system to investigate antioxidant activity and reported that the activity was slightly increased by an irradiation; however, at higher concentrations, the activity was reduced or was the same when compared with the nonirradiated phytic acid. Ahn and others (2004) also conducted a comparative study to evaluate antioxidant activities of irradiated phytic acid and commonly used antioxidants,including ascorbic acid,tocopherol,and butylated hydroxyl anisol (BHA). Phytic acid irradiated at 20 kGy showed a significantly higher DPPH radical scavenging activity than the ascorbic acid at the 800 μM level, whereas the scavenging effect was not observed in the nonirradiated phytic acid. Ferric reducing antioxidant power (FRAP) of phytic acid was significantly increased by irradiation. Fan and Thayer (2002) also

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observed an irradiation-induced increase in FRAP values in apple juice. Recently Park and others (2004) used a meat model system and found that irradiated phytic acid significantly inhibited lipid oxidation in meats when compared to the control and ascorbic acid treated samples during two weeks of refrigerated storage. The authors also suggested that irradiated phytic acid was effective in inhibiting the loss of the heme iron and metmyoglobin formation during storage, which, in turn, might improve antioxidant activity of phytic acid in meats (Park and others 2004).

Chlorophyll b Breakdown Chlorophylls not only cause an undesirable color change in vegetable oils but impair the hydrogenation process (Daun 1982) and promote oxidation in the presence of light, although they may be antioxidants under dark conditions (Abraham and deMan 1986). Oil sample containing 3 ppm of chlorophyll showed no detectable chlorophyll after being irradiated at 20 kGy either with or without N2 flush (Byun and others 2002c).The nonirradiated control sample stored in dark to avoid a photooxidation showed no change in chlorophyll levels during six hr storage. Results on peroxide values (POV) indicate that irradiation increased lipid oxidation but the chlorophyll breakdown in the sample irradiated at 20 kGy did not induce photooxidation when exposed to light. Irradiation of samples without oxygen (treated by continuous N2-bubbling) did not develop lipid oxidation during the irradiation process or photooxidation during storage under light (Byun and others 2002c).The POV value of 20 kGy-irradiated samples with N2-flushing remained at 0 during the entire storage regardless of lighting conditions, indicating that irradiation destroyed virtually all of the chlorophyll, resulting in a complete protection from photoxidation. The results suggested that irradiation of oils conducted in the absence of oxygen can be used to eliminate residual chlorophyll.

Color Improvement of Plant Extracts without Change of Biological Functions Green tea, one of the most popular beverages, is composed of about 30% of polyphenols (dry basis), such as flavanols, flavandiols, flavanoids, and phenol acids.The polyphenols are well known to have various excellent biological activities. In spite of all the beneficial effects, green tea leaf has been used mostly for brewing. This is mainly because of its deep dark

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color and off-flavor, which makes it very difficult to apply the proper amount in cosmetics, medicine, or foods. Studies of the feasibility of using irradiation to develop a new processing method to obtain a light-colored material that maintains its biological function have been conducted (Jo and others 2003a). Jo and others (2003a) reported that irradiation of 70% ethanol green tea exact showed higher Hunter color L*-value and lower a*- and b*-values, resulting in a color change of solution to bright yellow from dark brown. There was no difference in the radical scavenging and tyrosinase inhibition effect by irradiation. Similar results were obtained from a series of studies using different natural materials such as persimmon leaf (Diospyros kaki L. folium), licorice (Glycyrrhiza Uralensis Fischer) root (Jo and others 2003d) and its stolon, and Japanese honeysuckle (Byun and others 2004b). Jo and others (2003b) also applied the irradiated green tea leaf powder to raw and cooked pork patties. Results showed that addition of 0.1% extract to the patties decreased radical scavenging effect, resulting in a reduction of the lipid oxidation in raw and cooked patties. Recent publications have suggested that irradiated extracts from natural resources such as green tea leaf can be applied to the cosmetic industry because the functionality of cream lotion prepared from irradiated extract and commercial counterparts was similar (Byun and others 2004).

Application of Irradiation for the Development of Traditional Fermented Foods Various lactic acid–producing bacteria and yeast strains are responsible for the fermentation of Korean salted and fermented food (Byun and others 2000b; Lee 1997). However, after it reaches a well-ripened stage, the microbiological activities continue, resulting in sour and bitter taste, offodor, and softening due to deterioration of the fermented food (Cheigh and Park 1994). Therefore, inactivation of the fermentative microorganisms is essential for preservation and extending the shelf life of the fermented food. Recently, several studies have reported the significant effects of gamma irradiation on the microbiological control of fermented foods.Three groups of salted and fermented foods (fermented vegetables [Kimchi] [Song and others 2004], fermented fish [Jeotkal] [Byun and others 2000b; Jo and others 2004], and fermented soybean [Jang] [Byun and others 2002b; Kim and others 2002]) were examined. Irradiation has been reported to be effective in improving the quality and shelf-stability of fermented foods, although the effect of gamma irradiation on the fermentative microorganisms in each product was differ-

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ent. The D values of acid-forming bacteria, yeast and the Bacillus group were 1.0–3.0 kGy, 0.80–2.50 kGy, and 2.5–5.0 kGy, respectively.The large variation in D value was reported to be due to the differences in the microflora and environment among the products (Kim and others 2002; Song and others 2004). Although gamma irradiation inactivated the fermentative microbes effectively, the hydrolytic enzyme activity remained. Therefore, gamma irradiation can be applied not only for improving the quality and shelfstability but also for controlling the aging process of fermented foods (Song and others 2004). Effects of gamma irradiation on nutritional, physiological, and physicochemical properties of the fermented food were investigated and the results showed that generally, these properties were not influenced by gamma irradiation at 10 kGy (Byun and others 2002b; Jo and others 2004; Song and others 2004). However, the fermented foods irradiated up to 10 kGy had lower scores for their sensory acceptability than those of the control or irradiated at 2.5 and 5 kGy (Song and others 2004).Therefore, gamma irradiation at 2.5–5 kGy is recommended for the control of fermentation process and the improvement of the shelf life of salted and fermented foods. The salt content of the fermented food is high, generally 15 to 30%. Effects of gamma irradiation on low-salt fermented foods were studied. Results showed that gamma irradiation was effective for maintaining a better quality of low-salt fermented fish and soybean products.Although the suitable radiation dose in each low-salt product was different, the salt content of foods can be reduced by 25–50% when treated with gamma irradiation (Lee and others 2002; Jo and others 2004).

Conclusion Results indicate that food irradiation technology has a great potential to reduce or eliminate toxic or undesirable compounds in food. Further research is needed to identify the breakdown products induced by irradiation. Research on the effectiveness and feasibility of irradiation applications in real food systems is also needed. Finally, the quality of irradiated food or products should be studied to promote consumer acceptance.

Acknowledgements This study was supported by Korea Institute of Science & Technology Evaluation and Planning (KISTEP) and Ministry of Science & Technol-

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ogy (MOST), Korea government, through its National Nuclear Technology Program.

References Abraham V, deMan JM. 1986. Hydrogenation of canola oil as affected by chlorophyll. J Am Oil Chem Soc 63:1185–1188. Ahn HJ,Yook HS, Rhee MS, Lee CH, Cho YJ, Byun MW. 2002a.Application of gamma irradiation on breakdown of hazardous volatile N-nitrosamines. J Food Sci 67:596–599. Ahn HJ, Kim JH, Jo C, Lee CH, Byun MW. 2002b. Reduction of carcinogenic N-nitrosamines and residual nitrite in model system sausage by irradiation. J Food Sci 67:1370–1373. Ahn HJ, Kim JH, Jo C, Yook HS, Byun MW. 2003a. Radiolytic characteristics of nitrite by gamma irradiation. Food Chem 82:465–468. Ahn HJ, Kim JH,Yook HS, Byun MW. 2003b. Irradiation effects on free radical scavenging and antioxidative activity of phytic acid. J Food Sci 68:2221–2224. Ahn HJ, Kim JH, Jo C, Kim MJ, Byun MW. 2004. Comparison of irradiated phytic acid and other antioxidants antioxidant activity. Food Chem 173–178. Bartsch H, Oshima H, Pignatelli B. 1988. Inhibitors of endogenous nitrosation; mechanisms and implications in human cancer preservation. Mutat Res 202:307–324. Besler M, Steinhart H, Paschke A. 2001. Stability of food allergens and allergenicity of processed foods. J Chromatogr B Biomed Sci Appl 756:207–228. Bover-Cid S, Izquierdo-Pulido M,Vidal-Carou MC. 2000. Influence of hygienic quality of raw materials on biogenic amine production during ripening and storage of dry fermented sausages. J Food Prot 63:1544–1550. Byun MW, Lee JW,Yook HS, Lee KH, Kim KP. 1999.The improvement of color and shelf life of ham by gamma irradiation. J Food Prot 62:1162-1166. Byun MW, Kim JH, Lee JW, Park JW, Hong CS, Kang IJ. 2000a. Effects of gamma radiation on the conformational and antigenic properties of heat-stable major allergen in brown shrimp. J Food Prot 63: 940–944. Byun MW, Lee KH, Kim DH, Kim JH,Yook HS,Ahn HJ. 2000b. Effects of gamma radiation on sensory qualities, microbiological and chemical properties of salted and fermented squid. J Food Prot 63:934–939. Byun MW, Lee JW,Yook HS, Jo C, Kim HY. 2002a.Application of gamma irradiation for inhibition of food allergy. Radiat Phys Chem 63:369–370. Byun MW, Jo C, Lee KH, Kim KS. 2002b. Chlorophyll breakdown by gamma irradiation in a model system containing linoleic acid. J Am Oil Chem Soc 79:145–150. Byun MW, Jo C, Lee KH, Kim KS. 2002c. Chlorophyll breakdown by gamma irradiation in a model system containing linoleic acid. J Am Oil Chem Soc 79:145-150. Byun MW, Jo C, Lee JW, Jo SK, Kim KS. 2004.Application of radiation technology to develop green tea leaf as a natural resource for the cosmetic industry. Raidat Phys Chem 71:487–489. Byun MW, Jo C, Jeon TW, Hong CH. 2004b. Effects of gamma irradiation on color characteristics and biological activities of extracts of Lonicera japonica (Japanese honeysuckle) with methanol and acetone. Lebensm *Wiss u Technol 37:29-33. Chandra RK. 2002. Breast Feeding, hydroysate formulas and delayed introduction of selected foods in the prevention of food hypersensitivity and allergic disease. Nutr Res 12:125–135.

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Cheigh HS, Park KY. 1994. Biochemical, microbiological, and nutritional aspects of Kimchi (Korean fermented vegetable products). Critic Rev Food Sci Nutr 34:175–203. Chin KDH, Koehler PE. 1983. Identification and estimation of histamine, tryptamine, phenylethylamine, and tyramine in soy sauce by thin layer chromatography of dansyl derivatives. J Food Sci 48:1826–1828. Daun JK. 1982. The relationship between rapeseed chlorophyll, rapeseed oil chlorophyll and percentage green seeds. J Am Oil Chem Soc 59:15–18. Doudu KG, Minnaar A,Taylor IRN. 1999. Effect of cooking and irradiation on the labile vitamins and antinutrient content of a traditional African sorghum porridge and spinach relish. Food Chem 66:21–27. Fan X,Thayer DW. 2002. (n–1)Radiation influences browning, antioxidant activity, and malondialdehyde level of apple juice. J Agric Food Chem 50:710–715. Graf E, Eaton JW. 1990.Antioxidant functions of phytic acid. Free radical Biol Med 8:61–69. Harland BF, Harland I. 1980. Fermentative reduction of phytate in rye, white and whole wheat breads. Cereal Chem 57:628–633. Hates DJ, Murano EA, Murano PS, Olsen DG, Sapp SG. 1995. Food irradiation. Ames: Iowa State University Press, p. 71–73. Jeon GR, Lee JW, Byun MW, Lee SY. 2002. Reduced allergenicities of irradiated egg white ovalbumin determined by skin prick test and ELISA inhibition test. J Asthma Allergy Clin Immunol 22:711–719. Jo C, Son JH, Lee HJ, Byun MW. 2003a. Irradiation application for color removal and purification of green tea leaves extract. Radiat Phy Chem 66:179–184. Jo C, Son JH, Sohn CB, Byun MW. 2003b. Functional properties of raw and cooked pork patties with added irradiated, freeze-dried green tea leaf extract powder during storage at 4°C. Meat Sci 64:13–17. Jo C,Yook HS, Lee MS, Kim JH, Song HP, Kwon JS, Byun MW. 2003c. Irradiation effects on embryotoxicity and oxidative properties of gossypol dissolved in methanol. Food Chem Toxicol 41:1329–1336. Jo C, Son JH, Shin MG, Byun MW. 2003d. Irradiation effects on color and functional properties of persimmon (Diospyros kaki L. folium) leaf extract and licorice (Glycyrrhiza Uralensis Fischer) root extract during storage. Lebensm –Wiss u –Technol 67:143–148. Jo C, Lee WD, Kim JH, Kim Ahn, HJ, Byun MW. 2004. Quality attributes of low-salt Changran Jeotkal (aged and seasoned intestine of Alaska Pollock,Therage chalcogramma) developed using gamma irradiation. Food Control 15:435–440. Joosten HMLG. 1988.The biogenic amine contents of Dutch cheese and their toxicological significance. Neth Milk Dairy J 42:25–42. Kim DH, Jo C,Yook HS, Park BJ, Byun MW. 2002. Enhancement of preservation characteristics of Meju, and intermediate material for Korean legume-based fermented soy sauce, Kanjang, by irradiation. Radiat Phys Chem 64:317–322. Kim DH, Song HP,Yook HS, Ryu YK, Byun MW. 2004. Isolation of enteric pathogens in the fermentation process of Kimchi (Korean fermented vegetables) and its radicidation by gamma irradiation. Food Control 15:441–445. Kim JH,Ahn HJ, Kim DH, Jo C,Yook HS, Park HJ, Byun MW. 2003. Irradiation effects on biogenic amines in Korean fermented soybean paste during fermentation. J Food Sci 68:80–84. Larson SR, Rutger IN, Young KA, RAboy V. 2000. Isolation and genetic mapping of a nonlethal rice (Oryzae sativa L.) low phytic acid mutation. Crop Sci 40:L397–405. Lee CH. 1997. Lactic acid fermented foods and their benefits in Asia. Food Control 8:259–269.

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Lee JW,Yook HS, Lee KH, Kim JH, Byun MW. 2000. Conformational changes of myosine by gamma irradiation. Radiat Phy Chem 58:271–277. Lee JW,Yook HS, Cho KH, Lee SY, Byun MW. 2001a.The changes of allergenic and antigenic properties of egg white albumin (Gal d l) by gamma irradiation. J Korean Soc Food Sci Nutr 30:500–504. Lee JW, Kim JH,Yook HS, Kang KO, Lee WY, Hwang HJ, Byun MW. 2001b. Effects of gamma radiation on the allergenicity and antigenicity properties of milk proteins. J Food Prot 64:272–276. Lee KH, Ahn HJ, Jo C, Yook HS, Byun MW. 2002. Production of low salted and fermented shrimp by irradiation. J Food Sci 67:1772–1777. Metchlfe DD, Sampson HA, Simon RA. 1997. Food allergy: Adverse reactions to foods and food additives, Blackwell Science, U.S.A. Mine Y, Sasaki E, Zhang JW. 2003. Reduction of antigenicity and allergenicity of genetically modified egg white allergen, ovomucoid third domain. BBRC 302:133–137. Nout MJR, Ruiker MMW, Bouwmeester HM. 1993. Effect of processing conditions on the formation of biogenic amines and ethyl carbarnate in soybean tempe. J Food Safety 33: 293–303. Novitch M. 1983.Action levels for total volatile N-nitrosamines in rubber baby bottle nipples: availability of compliance policy guide. Fed Reg 48:57014. Olsen K, Kristiansen KR, Skibsted LH. 2003. Effect of high hydrostatic pressure on the steady-state kinetic of tryptic hydrolysis of ß-lactoglobulmin. Food Chem 80:225–260. Park HR, Ahn HJ, Kim JH, Yook HS, Kim S, Lee CH, Byun MW. 2004. Effects of irradiated phytic acid on antioxidation and color stability in meat models. J Agric Food Chem 52:2572–2576. Reddy NR, Pierson MD, Sathe SK, Salunkhe DK. 1989. Phytates in cereals and legumes. Boca Raton, FL: CRC Press. 152 p. Rickard SE, Thompson LU. 1997. Interactions and biological effects of phytic acid. In: Shahidi F, ed.Antinutrients and phytochemicals in foods.ACS symposium series, no 662. Washington, D.C.:American Chemical Society. p 294–312. Sampson HA. 2004. Update on food allergy. J Allergy Clin Immunol 113:805–809. Seel DJ, Kawabata T, Nakamura M, Ishibashi T, Hamano M, Mashimo M, Shin SH, Sakamoto K, Jhee EC,Watanabe S. 1994. N-nitroso compounds in two nitrosated food products in southwest Korea. Food Chem Toxicol 32:1117–1123. Seo JH, Lee JW, Lee YS, Lee SY, Kim MR,Yook HS, Byun MW. 2004. Change of an egg allergen in a white layer cake containing gamma-irradiated egg white. J Food Prot 67:1725–1730. Shalaby AR. 1996. Significance of biogenic amines to food safety and human health. Food Res Int 29:675–690. Shamsuddin AM,Vucenik I, Cole KE. 1997. IP6:A novel anti-cancer agent.Life Sci 61:343–354. Shuker DEG,Tannenbaum SR. 1983. Determination of nonvolatile N-nitroso compounds in biological fluids by liquid chromatography with postcolumn photohydrolysis detection.Anal Chem 55:2152–2155. Siddhuraju P, Makkar HPS, Becker K. 2002.The effect of ionizing radiation on antinutritional factors and the nutritional value of plant materials with reference to human and animal food. Food Chem 78:187–205. Silla Santos MH. 1996. Biogenic amines: their importance in foods. Int J Food Microbiol 29:213–231. Song HP, Kim DH,Yook HS, Kim KS, Kwon JH, Byun MW. 2004.Application of gamma irradiation for aging control and improvement of shelf-life of Kimchi, Korean salted and fermented vegetables. Radiat Phys Chem 71:55–58.

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Svenning C, Brynhildsvold J, Molland T, Langsrud T,Vagarud GE. 2000.Antigenic response of whey proteins and genetic variants of ß-lactoglobumin the effect of proteolysis and processing. Int Dairy J 10:699–711. Tricker AR, Spiegelhalder B, Preussmann R. 1989. Environmental exposure to performed nitroso compounds. Cancer Surveys. 8:251–259. Vermeer ITM, Moonen EJC, Dallinga JW, Kleinjans JCS, Maanen MS. 1999. Effects of ascorbic acid and green tea on endogenous formation of N-nitrosodimethylamine and N-nitrosopiperidine in humans. Mutat Res 428:353–361. Wierbicki E, Brynjolfsson A. 1979. The use of irradiation to reduce or eliminate nitrite in cured meats. Paper presented at 25th European Meeting of Meat Research Workers, Budapest, Hungary. WHO. World Health Organization. 1999. High-dose irradiation: Wholesomeness of food irradiated with doses above 10 kGy.WHO Technical Report Series 890. Geneva. Yang CS,Wang ZY. 1993.Tea and cancer. J Nat Cancer Inst 85:1038–1049. Zou XN, Lu SH, Liu B. 1994.Volatile N-nitrosamines and their precursors in Chinese salted fish-A possible etiological factor for NPC in China. Int J Cancer 59:155–158.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 16 A FUTURE UNCERTAIN: FOOD IRRADIATION FROM A LEGAL PERSPECTIVE Denis W. Stearns

Introduction Food irradiation is not a new technology; its effectiveness in killing microbes in food has been known for more than 80 years.1 It is estimated that 500,000 tons of food are irradiated each year around the world.2 Yet, in the United States, the GAO reports that the amount of food irradiated each year represents a “tiny fraction of the total amount of food consumed.”This is so despite the fact that the CDC estimates that irradiating meat and poultry could prevent nearly a million cases of foodborne illness, 8,500 hospitalizations, more than 6,000 catastrophic illnesses, and 350 deaths in the United States each year.3 There are numerous and conflicting factors that could explain why the food industry has not adopted irradiation as a preventive technology. These factors include technical feasibility, the high capital costs of irradiation equipment, the reluctance to be a first-mover in a competitive, lowprofit-margin industry, a market limited by consumer concerns, and a wide variety of other economic disincentives for safety-related process innovation.4 Viewed from a legal perspective, which is to say the perspective of an attorney practicing in this area, the industry’s failure to adopt irradiation technology, or to widely use irradiated products, is more difficult to explain. Indeed, to the plaintiff attorneys who handle the majority of food product cases filed each year, the extremely limited use of irradiation in the food industry is extremely puzzling.5 263

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Food irradiation has the capacity to substantially reduce not only the risk of lost sales that result from an outbreak or recall but also the lawsuits that inevitably follow.The filing of these lawsuits is nearly always accompanied by significant and sustained media attention, most of it negative. Moreover, during the course of litigation, news about the outbreak continues to come out, often depressing sales and the company’s stock price. For example, in the year that litigation arising from a Salmonella outbreak linked to a Chicago-area restaurant was pending, the value of the company’s outstanding shares fell by sixteen percent, for a loss of a half billion dollars.6 Given that there is rarely, if ever, an effective legal defense against an outbreak-related foodborne illness claim, one might reasonably assume that manufacturers and restaurant owners would adopt food irradiation, or the use of irradiated food, as a means of reducing their lawsuit-related risk exposure. But that has certainly not occurred. Nonetheless, when viewing the issue of food irradiation from a legal perspective, three preliminary conclusions can be reached. First, the widespread adoption of irradiation technology is unlikely to occur based on legal incentives in the absence of a regulatory mandate or customer demand for a safer product linked to a specific acceptance of irradiation. Second, a legal duty to irradiate already exists with regard to susceptible populations, and the legal consequences associated with the breach of this duty may turn out to be the primary driver of greater consumer acceptance of irradiated food products.Third, the question of whether food irradiation poses any long-term safety risk to the consumer raises the possibility of future legal liability that acts as a further disincentive to the adoption of the technology.

Liability for the Manufacture of a Defective Food Product There is a commonly held misconception in the food industry.That misconception is that liability for a product-related injury requires proof of negligence.7 As a result, it is assumed that if a person injured by a product wants to sue to recover damages, she must be able to present evidence that the product was defective because the manufacturer failed to use reasonable care in making it. It is further assumed that if a person cannot come up with such evidence, or if the manufacturer can prove it acted as carefully as possible, the lawsuit will fail. These assumptions, however, represent wishful thinking on the part of food industry. The rule that governs the right to recover for product-related injury is decidedly stricter than is often assumed. Indeed, the rule is called strict

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liability for a reason; it is liability without regard to fault.And, at present, some form of strict liability exists in all 50 states.8 The Origins of Strict Liability in Tainted Food Cases The rule of strict liability has its roots in the judicial creation of a legal remedy for people injured by unsafe food.9 The seminal case is a 1913 decision by the Washington Supreme Court, Mazetti v. Armour & Company.10 It has been called “one of the most important cases in the development of early twentieth century product law in the United States.”11 The case involved canned tongue that had somehow gone foul, causing the person who ate it to become quite sick. In holding that the injured person could sue the manufacturer, even though it had no contractual relationship with it, the court recognized that there exists in law an implied warranty (or promise) that all food sold is fit for consumption, and that, when it is not, the manufacturer is liable for the injury so caused. This new rule was said by the court to be necessary due to the “modern method of preparing food for use by the consumer, and the more general and ever increasing use of prepared food products.” The rule was also premised on what it called “the demands of social justice.” The law was being forced to catch up with the rise of mass production and broader distribution of consumer products. A new relationship between producer and user was emerging, and the courts were being called upon to grapple with the socio-legal implications.12 Whereas previously a person might grow his own food, or buy food from someone with whom he had a personal relationship in a face-to-face dealing, now packaged food came from myriad sources with nothing to identify the maker except brand names. For this reason, brand names came to be trusted as guarantees of consistent product quality—so much so that even now consumers prefer branded over nonbranded products because they reduce concerns about product quality.13 The Modern Rule of Strict Liability The modern rule of strict liability was first announced by a court in 1963 in a case that involved a defective power tool.The case was Greenman v.Yuba Power Products, and it did away with the legal fiction that a manufacturer’s liability for injury was based on the implied promise that the product was safe to use.14 Writing for the California Supreme Court, Chief Justice Roger Traynor, widely considered a father of product liability law, stated that it was “clear that the liability is not one governed by the law of contract warranties but by the law of strict liability in tort.”

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Under this new rule of strict liability, to hold a manufacturer liable, a person injured while using a product need show only that: (1) the product was defective; (2) it was used as intended; and (3) the defect caused the injury.The care used in the manufacture of the product is irrelevant to the determination of liability.The only issue in a product liability case is the defectiveness of the product, not the manufacturer’s conduct in somehow allowing the defect to come into existence. As a result, proof of negligence is not required to recover damages in a product defect case. And although strict liability has given rise to controversy in other contexts, there has been little if any when applied to food.15 Defining Products and Defects There are three kinds of product defects that give rise to strict liability: manufacturing defects, design defects, and marketing claims. Food injury claims primarily involve manufacturing defects, the most straightforward and uncontroversial of product claims. As one commentator has aptly pointed out, when talking about a manufacturing defect, the need for a definition is not obvious. For decades, both courts and commentators considered the meaning of the “manufacturing defect” concept so selfevident as to be self-defining.16 The inquiry into whether a product is defective closely coincides with common sense. A product is defective for not being used how it was supposed to be. Put in more strictly legal terms, the product is not reasonably safe in construction because, as one state legislature has defined it, “the product deviated in some material way from the design specifications or performance standards of the manufacturer, or deviated in some material way from otherwise identical units of the same product line.”17 This is in marked contrast to design and marketing defect cases in which the defective products are said to be “generically dangerous,” because every product unit designed and marketed in the same way shares the same risk potential.18 The risks associated with an entire product line are, as a result, potentially charged to the manufacturer.19 Proving the Existence of a Defect in Food Just as it is commonly assumed that proof of negligence is required to establish liability for a product-related injury, so it is equally commonly assumed that proving the existence of a defect is difficult in food cases.20 This assumption might seem reasonable, at first glance, because food products are typically destroyed—that is, eaten or discarded—and thus

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direct evidence of the defect rarely exists. Fortunately for the injured person, direct evidence is not required to prove the existence of a product defect, or precisely how or why the product failed. In manufacturing defect cases the fact of product malfunction, and resulting injury, is by itself enough to give rise to a presumption of negligence and thus liability in most states.This is sometimes referred to as the malfunction doctrine.21 Its fundamental premise is the high correlation between the existence of a defect and a failure of some kind in the manufacturing process.22 This makes the issue of negligence not worth the cost and uncertainties of trying to prove.Thus, in the case of a manufacturing defect, it is simply not a useful exercise to ask whether the defect could have been prevented; the existence of the defect is by itself sufficient to impose liability. For cases involving unsafe food, it is nearly always a manufacturing defect at issue, especially when pathogens such as E. coli O157:H7, Salmonella, or hepatitis A are involved.And although it is true that a manufacturer is not liable for a product-related injury unless the product is both defective and unsafe, in food cases this is a distinction without a difference. Food that is unsafe because it is unfit to eat is by definition defective. For that reason, it is rare to have a defendant in a food contamination case dispute liability unless there is a serious question of causation, or some other product-related problem of proof.23 Moreover, because only cases with problems of proof, or uncertain damages, tend to go to trial, this would explain the low win percentage for plaintiffs who go to trial, and the relatively small damage awards for those cases the plaintiffs do win.24 In short, unless a defendant acts irrationally, defective food cases nearly always settle.

Strict Liability Creates Few If Any Legal Incentives in Favor of Food Irradiation The rationales supporting the rule of strict liability are hotly debated.25 That is, except when it comes to food cases.As noted by one group that exhaustively studied the topic: Although the doctrine of strict liability (or recovery without proof of fault on the part of the seller) is controversial in some contexts, it has not elicited any substantial outcry with respect to food-related harms.26 One reason for this lack of controversy is the primacy the public gives to food safety, particularly when it comes to microbial contamination. In

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one study, the number one food safety concern cited was the risk of contamination by bacteria or other microorganisms.27 Another reason for the lack of controversy is that manufacturers have near-exclusive access to the information needed for the effective control of product hazards. Strict liability is therefore intended to motivate manufacturers to use the information to reduce the occurrence of productrelated accidents.28 In addition to the information advantage they possess over consumers, manufacturers also get to make a deliberate choice about the level of investment in production quality and control processes.29 Certainly, many of these choices are dictated by regulatory regimes such as those that require USDA-inspected meat-processing facilities to adopt HACCP plans.30 But even so, the details of such plans, including the technologies used, remain solely in the control of the manufacturer. As a result, the fact that a plant is federally inspected and its HACCP plan required as a matter of regulatory law provides no legal defense to a strict liability claim, despite the meat industry’s continuing arguments to the contrary.31 Consequently, when it comes to food irradiation it is reasonable to ask why the continued prevalence of foodborne illness outbreaks has not given rise to the greater adoption of this technology. The USDA’s Economic Research Service has looked at the issue from an economic perspective without finding any one answer.32 It has also looked at incentives to food safety from the perspective of product liability, concluding in part that a lack of information about the true costs of food-related litigation prevented anything but educated guesses.33 A national committee on ensuring safe food concluded the same thing.34 From the perspective of the attorneys who have handled the majority of food defect cases over the last several years, it appears that resistance to irradiation and other innovative preventive technologies is in part the result of a kind of corporate denial of risk.Time after time it seems that only the benefit of hindsight motivates companies to act, even when the risk was foreseen and preventable. For example, something as simple as the scheduled replacement of water heaters would likely have been enough to prevent the Salmonella outbreak at a Chicago-area restaurant closed when sales did not recover. But the investment in this policy change did not occur until after the outbreak happened, too late for those injured in it. Improvements accomplished after an accident are something that the law has long taken into account. For example, evidence of “subsequent remedial measures” is not admissible at trial “to prove negligence, culpable conduct, a defect in a product, a defect in a product’s design, or a need for a warning or instruction.”35 The reasons for the Rule are many,

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but the most notable and widely accepted one rests on a social policy of encouraging people to take, or at least not discouraging them from taking, steps that advance safety.36 Although the doctrine of strict liability is supposed to create a similar kind of encouragement of improved product safety, it is not at all clear that the doctrine has had that effect in the food industry. Recall that the great reforms of the early twentieth century were prompted in large part by Upton Sinclair’s throwing open the doors of the slaughterhouse and showing the public what really went on inside there.37 With the rise of strict liability and its easing of the burden of proof on the issue of product defect, the focus is no longer on how the manufacturer acted.And although this is a good thing for those injured by defective products, because it nearly guarantees them a recovery that they might not otherwise have received, it remains open to question whether strict liability might be more disincentive than incentive when it comes to the adoption of expensive preventive technologies. On the other hand, as expertise in food-related litigation continues to be concentrated in one or two law firms, there may yet be a tipping point that results in the availability of new information that would allow the more thorough and accurate analyses that most agree are necessary to ensure improved food safety.The number of confidential settlements may decrease as attorneys representing plaintiffs refuse to agree to them. More and better cases may start going to trial with verdicts becoming part of the public records.And as discussed further below, plaintiffs may begin to increasingly seek punitive damage awards for which there is no insurance coverage available, thus causing greater economic harm to companies who fail to adopt available food safety innovations. In sum, although legal liability may in the short term be a relatively weak incentive to proactive improvement in food safety, its potential remains largely untapped.Therefore, as with so many things, time will tell.

A Possible Existing Legal Duty to Use Irradiated Food: The Challenge of Highly Susceptible Populations We know that not all segments of the population are equally at risk for infection with a foodborne pathogen. Organisms that a healthy immune system might otherwise fight off pose a greater risk to someone whose immune system is impaired. Consequently, one major identified factor contributing to the emergence of foodborne disease in the United States is a significant annual increase in the proportion of the population with decreased or impaired immune function.38 The members of these so-

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called “highly susceptible populations” include the elderly, preschool age children, persons with AIDS or infected with the HIV virus, and anyone else immunocompromised as a result of chronic disease, chemotherapy, or organ-transplantation.39 Because it is clear that the size of the highly susceptible population is certain to grow, the food industry has no choice but to take this increasing risk into account when making decisions about what, if any, additional steps to take to prevent a parallel increase in the incidence of foodborne illness attributable to its product. Failing to take action is likely to otherwise result in a potentially significant increase in litigation. Negligence: Failing to Avoid a Known and Avoidable Risk Negligence is the failure to exercise ordinary care.What defines ordinary care is in most cases knowledge of the risk. Actual knowledge is not required, however.The law attributes to one who acts both what is known and what should be known or have been discovered. In other words, ignorance is no defense where the facts known or available would have alerted a reasonable person to the likelihood of danger. When dealing with a strict liability claim involving a manufacturing defect, we know that proof of negligence is not required. This does not mean, though, that there is no fault; it means only that the plaintiff need not prove fault to hold the manufacturer liable for her damages.And because a manufacturer cannot be held liable more than once and so provide an injured person with a kind of double-recovery, proving the elements of negligence, in addition to the elements of strict liability, gains nothing.That said, there are times when proof of negligence is necessary, as in when the entity being sued is not a manufacturer, and strict liability does not apply. Say, for example, you are a resident of an assisted-living facility and, as part of the services provided for a monthly fee, you have access to a dining room where three meals per day are served.The meals are prepared on-site by employees of the facility. One morning you are given eggs benedict with hollandaise sauce made from unpasteurized shell eggs.You eat the meal, are infected with Salmonella, and after a lingering, painful illness, you die. Assuming that the owner of the facility is not deemed a manufacturer, and the deadly breakfast not a product, then a case for negligence would need to be made.And given these facts, it would be an easy case to make. The risk associated with the use of unpasteurized eggs in food establishments that serve a highly susceptible population is by now well established and understood.The publication of the 2001 FDA Food Code gave

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this standard of care the equivalent of the force of law. Even in jurisdictions that do not adopt the standard, an establishment failing to follow the standard would likely find its conduct impossible to justify if such failing caused injury or death.The risk was known and the means to avoid it was available at little cost relative to the harm. Because the use of pasteurized fruit juice and eggs with highly susceptible populations is now essentially mandatory, it is not surprising that the use of irradiated food in therapeutic diets fed to immunocompromised patients in health care facilities is one area in which we see greater acceptance of such products.40 What is surprising, however, is that people who are at increased risk of foodborne illness do not themselves seem more willing to buy irradiated products.41 When the use of pasteurized and irradiated food products in a therapeutic setting is admitted to be a legal (and arguably ethical) no-brainer, the question then arises why these products are not used in every setting where there is a high likelihood of there being consumers who are members of highly susceptible populations? That was a question faced by the FDA as it considered whether to make mandatory the safe egg handling and preparation practices in its 2001 Model Food for all retail establishments that serve a highly susceptible population.42 But as several of the comments submitted on the proposed rule pointed out, it does not make a lot of sense to protect highly susceptible populations in one setting, but not another, when their presence, as a general matter, is equally foreseeable given their numbers. The Eggshell Plaintiff: Irradiation, Liability, and Susceptible Populations Some might argue that it is unfair to hold a company liable for the full extent of a person’s injuries when the largest part of those injuries can be attributed to the fact that the person was immunocompromised or otherwise in frail condition. This argument has no support in the law, however. In the first year of law school one of the truisms that all students learn is that the defendant takes the plaintiff as she comes.This is referred to as the eggshell or thin-skulled plaintiff rule, and it holds that a defendant is liable for all injuries caused by its negligent conduct, even when it has the misfortune of having a plaintiff particularly susceptible to severe injuries or even death. There are also cases in which there exists a relatively small group of people with outsized and, arguably, unpredictable reactions to the exposure to, or use of, a product otherwise safely used by millions of others.

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In these cases the question sometime becomes whether the product is, in fact, defective. Latex gloves are one example of a product that was found by a jury to be defective even though they contained no impurities and were dangerous only as a result of an allergic reaction by the user.43 Although noting that there is not usually recovery when the reaction to the product is “idiosyncratic” and “extremely rare,” in this case the court found that such a rule does not act as an innate bar to recovery in every allergic reaction case. Instead, the question of defectiveness would have to be determined on a case-by-case basis considering the magnitude of danger necessary to render a product dangerous to an extent beyond which would be contemplated by the ordinary consumer. Such an evaluation done with regard to the use of irradiated food with susceptible populations would seem to result in but one conclusion: a nonirradiated product when intended for consumption by a susceptible person is an unreasonably dangerous product.Therefore, once more we are driven to the conclusion that failure to use an irradiated food product when it is reasonably likely that the failure will result in injury or death constitutes negligence. The Prospect of Punitive Damages As a Stronger Incentive The circumstances that apply to a negligence claim may also apply to a claim for punitive damages. Also known as exemplary damages, these claims are typically premised on conduct that represents a “conscious and knowing disregard” or a “conscious indifference” to a known safety risk.44 Although many have argued that punitive damages are inconsistent with strict liability and its focus on the product, not conduct, this argument has not gained wide acceptance in the courts.This is because the conduct proved in punitive damage cases is of a nature easily deemed outrageous and thus worth both punishing and deterring. The injured person is therefore entitled to a kind of windfall award of damages, above what is needed for compensation, as an inducement to bring “malefactors to justice.”45 Punitive damages are most often awarded in product cases in which there is evidence that a company deliberately chose to expose consumers to serious risks against which they have no good way to defend. This would typically be instances in which the defect is not obvious. Combine this with evidence of a strong profit motive and you have a case in which punitive damages are likely to be upheld, although not in every case. In the case of irradiated food, there seems little question that the failure to use it in a therapeutic setting would constitute a conscious disregard of a known risk, because we know that irradiation can eliminate mi-

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crobial pathogens from ready-to-eat food products, fresh vegetables, meat, and poultry.46 We also know that immunocompromised people are at greater risk for infection with a foodborne disease, as well as at greater risk for more serious injury or death as a result of the infection.47 Combine such knowledge with evidence that irradiation adds only pennies per pound to the cost of food and it is likely that most juries would have no difficulty awarding punitive damages against, for example, the operator of a nursing home that chose to use a cheaper, but demonstrably more dangerous, nonirradiated product. The size of punitive damage awards is notoriously difficult to predict, and often rests on jury outrages as much as anything else. For example, in 2002, a jury in Nevada awarded five guests of the Reno Hilton $22,000 for the injuries suffered as a result of outbreak-related norovirus infections.48 The plaintiffs had argued that an award of punitive damages was justified because the hotel had acted in outrageous fashion by not having a paid sick-leave policy and knowingly allowing sick workers to keep working. The jury obviously agreed because it awarded the plaintiffs $25.2 million in punitive damages. Given the enormity of the risk and its unpredictability, the prospect of a punitive damages award should act as a strong incentive for the use of irradiated food where the establishment serves highly susceptible populations. Although such an award has not yet occurred, its occurrence is probably, again, just a matter of time. And when it does occur, whatever institutional resistance to the use of irradiated food still exists is likely to disappear at a rapid pace.This then might also spur others in the food industry to revise their own risk assessments, especially in light of the increasing numbers of immunocompromised persons in all settings.

The Possibility of Liability Arising from Irradiated Foods There is no question that the irradiation of food remains a controversial topic, and the primary source of the controversy is concern over the long-term health effects of consuming irradiated food.This controversy is stoked by organizations such as Public Citizen and Center for Food Safety, which actively oppose FDA and other agency efforts to allow increased use of irradiation in the manufacture of foods.49 These groups argue that official governmental reviews have “whitewashed” the potentially serious public health concerns that will become more serious if a larger portion of the food supply is irradiated. Some even speak of a looming “epidemic of cancer” attributable to the chemical byproducts created by irradiation in meat.

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Not surprisingly, this vocal opposition to food irradiation does not appear to represent the views of a majority of consumers.50 Opinion surveys and consumer research consistently show that people will purchase irradiated food, and that acceptance increases markedly when potential purchasers are knowledgeable about both the process and food safety risks it prevents. Nonetheless, the perception of far greater resistance than might actually exist appears to have undercut the willingness of manufacturers to market irradiated food products on anything but a small-scale or test basis.This has prompted two leading public health officials to blame the public health community for being silent for so long on the issue, and to question “why the food industry has not stepped into the vacuum created by this lack of leadership from public health,” especially when “[f]aced with the liability of marketing hazardous foods.”51 There are two probable and complementary answers to this question. First, the food industry appears unwilling to be frank about the risks posed by its products as a means of educating the consumer about the need for irradiation. To talk about the significant public health benefits that would derive from irradiation of meat and poultry, the industry would require the food industry to talk about the illness and death presently caused by its products, something that it is understandably reluctant to do. Second, the food industry apparently prefers to move beyond the controversy by moving beyond the use of the term “irradiation” altogether. By using the term “cold pasteurization,” the industry hopes that the already accepted technology of pasteurization will act as a proxy for acceptance of irradiation under a new name. Some might call this a “bait-and-switch” tactic, but it is better characterized as a simple attempt to avoid the question of the long-term safety of eating irradiated food. Trying to gain acceptance with a name change, rather than forthrightly defending both the safety of irradiation and, more important, the need for it, plays into the hands of those who are accusing the government and the food industry of trying to whitewash the dangers. It is not enough to criticize opponents of food irradiation solely by way of an analogy to earlier, and unfounded, objections to milk pasteurization.52 For even if this analogy appears by all evidence to be apt, it is not a complete rebuttal. Moreover, the history of litigation is replete with products once deemed safe that turned out years and even decades later to have been dangerous. Consider, for example, asbestos. Asbestos was widely used and considered safe before being linked to massive numbers of illness and deaths caused by long-term exposure to the product.53 The resulting litigation pushed most asbestos manufacturers into bankruptcy or out of existence.And this litigation, which started in earnest in 1973 with a federal court decision finding asbestos manu-

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facturers strictly liable to workers injured as a result of exposure to their products, is still going on today. The food industry is no doubt mindful, just as the public is, of the doubts being expressed about the safety of food irradiation.Therefore, irradiated food will likely continue to be used primarily as ingredients in products that require a higher level of safety or quality assurance, because no label informing the consumer of such use is required. Other than that, most companies will be content to wait and see, waiting on a substantial increase in consumer acceptance and allowing others in the food industry to become first adopters.

Conclusion The law has been aptly characterized as a “choosing system, in which the individuals can find out, in general terms at least, the costs they have to pay if they act in certain ways.”54 In the case of the food industry and irradiation, such costs will continue to be difficult to predict, and most often found out after the fact. In the absence of a regulatory mandate, such as that which occurred with the pasteurization of milk, the use of irradiation in the manufacture of food is likely to remain dependent on consumer acceptance and demand.The sole exception will be food products intended for consumption by highly susceptible populations where safety and liability risks are high, and resistance is minimal or nonexistent. Of course, if subsequent research demonstrates that irradiation is not as safe as it presently seems, then adoption and use of the technology will come to a swift halt, and a wave of litigation possibly like that seen with asbestos may result.

References* *References specially formatted for use by attorneys. 01. R. Tauxe, Food Safety and Irradiation: Protecting the Public from Foodborne Infections, EID 7(3); 516–21. 02. GAO Report, FOOD IRRADIATION:Available Research Indicates That Benefits Outweigh Risks,August 2000, available at http://www.gao.gov/archive/2000/rc00217.pdf. 03. Tauxe at p. 519, supra at Note 1. 04. For an excellent discussion of the economics of food safety innovation, see E. Golan, et al., Food Safety Innovation in the United States: Evidence from the Meat Industry, Economic Research Service/USDA, AER No. 831 available online at www.ers.usda. gov/Publications/aer831/. For a related discussion focusing on equipment costs and consumer concerns, see P. Frenzen et al., Consumer Acceptance of Irradiated Meat and Poultry in the United States, Jnl. Food Prot. 64(12); 2020–2026, and specifically

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05.

06. 07.

08.

09. 10. 11. 12.

13. 14.

15.

16. 17. 18.

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with regard to ground beef, R.M. Morrison, J.C. Buzby, & C.T. Jordan Lin, Irradiating Ground Beef to Enhance Food Safety, Food Review, 33–37, January-April 1997. The author is a principal in Marler Clark, a law firm that for the last seven years handled most of the more prominent foodborne illness cases in the United States. For a partial list of cases, see www.marlerclark.com/foodlitigation.htm Barry Michaels, Ph.D. Personal correspondence, 2005. Personal observations of the author and his partners at Marler Clark.As presenters on legal issues at up to twenty industry-sponsored or related conferences and meetings per year, we have been frequently confronted, especially during question-and-answer periods, by persons expressing shock that their company could be sued for a productrelated injury despite their ability to prove that they took every possible precaution. Restatement (Third) of Torts: Product Liability 1 (1998). Not all states, however, call it strict liability. For example, in Michigan, such liability is still treated as a form of implied warranty. See, e.g., Vincent v. Allen Bradley Co., 95 Mich.App. 426, 291 N.W. 2d 1 (1986) (holding that a breach of implied warranty is established on proof of injury caused by a defect in the product, attributable to the manufacturer, that made the product not reasonably fit for its intended use). D.G. Owen, Manufacturing Defects, 53 S.C. L. Rev. 851 (Summer 2002). For a concise but thorough overview of product liability law as it applies to food, see pp. 884–904. 135 Pac. 633 (Wash. 1913). M. Shapo, The Law of Product Liability, ¶ 6.01[2] (3d Ed. 1994). For an interesting, if somewhat overly philosophical and at times impenetrable, discussion of the relationships we can have with products, see A. Bernstein, How Can a Product Be Liable, 45 Duke L.J. 1 (October, 1995). Golan at p. 6, supra at Note 4. 377 P.2d 897 (Cal. 1963). Justice Traynor’s decision in Greenman v. Yuba Power Products anticipated the inclusion of the rule in the Restatement (Second) of Torts, the American Law Institute’s exhaustive survey of the common law.The rule was set forth at Section 402A, leading to strict liability being often referred to as “Section 402A liability.” Committee to Ensure Safe Food from Product to Consumption. Ensuring Safe Food from Production to Consumption, at 33, National Academy Press, 1998 (hereinafter Safe Food Committee).The exception to this is for the most part confined to cases involving raw meat products in which the industry’s position continues to be that it is the consumer’s responsibility to make raw meat safe to eat.To its credit, the USDA has rejected the meat industry’s position on consumer responsibility, stating that “[b]ecause industry has the means to reduce the risk or eliminate the hazard, consumers should not be expected to assume all responsibility for preventing foodborne illness associated with E. coli O157:H7.” See “Recent Developments Regarding Beef Products Containing E. coli O157:H7,” FSIS Docket No. 99-060N65, Fed. Reg. 6881, at 6884 (Feb. 11, 2000). Owen at p. 865, and 894, supra at Note 9. Revised Code of Washington, 7.72.030(2)(a)(defining one standard of strict liability for a product manufacturer). The term was coined by Professors James A. Henderson, Jr., and Aaron D. Twerski in Doctrinal Collapse in Products Liability: The Empty Shell of Failure to Warn, 65 N.Y.U. L. Rev. 265, 272 (1990) (stating that “after years of frustration, many courts have finally abandoned the search and declared that, for all intents and purposes, strict liability, as applied to generically dangerous product cases, was simply negligence by another name”).

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19. W. Kip Vicusi, Wading Through the Muddle of Risk-Utility Analysis, 39 Am. U.L. Rev. 573, 574 (Spring 1990). 20. See, e.g., S. Lassiter, From Hoof to Hamburger: The Fiction of a Safe Meat Supply, 33 Willamette L. Rev. 411, at 418 (1997), where the author argues, incorrectly, that “monetary awards are low because of the limited success in establishing a breach in the meat producer’s duty to produce meat that is safe for human consumption.” 21. Owen at p. 877–874, supra at Note 9.This doctrine is usually understood as a variation on the doctrine of res ipsa loquitor, which means “the thing speaks for itself”. 22. G. Schwarz, New Products, Old Products, Evolving Law, Retroactive Law, 58 N.Y.U. L. Rev.796, 810 (1983). 23. Owen at pp. 855–856 and fn. 27, supra at Note 9.The food cases at Marler Clark have consistently borne this out. See, e.g., Almquist v. Finley School District, 57 P.3d 1191 (2002) (conceding E. coli O157:H7 in a school lunch taco meat would make it defective but denying that the taco meat was the cause of the outbreak in question). 24. J.C. Buzby et al., Product Liability and Microbial Foodborne Illness, Economic Research Service/USDA, AER-799, at pp. 13–23 (noting that, of 175 foodborne illness lawsuits that went to verdict from 1988–1997, only 31.4% were won by plaintiffs, and the median damage award was $25,560). 25. Bernstein at pp. 5–6 and footnotes 14–16, supra at Note 12 (noting how the subject had become “overtly politicized” and citing the range of opinions among commentators). See also J. Henderson, Why Negligence Dominates Tort, 50 UCLA L. Rev. 377, 394 (December 2002) (noting that “American torts scholarship divides along several lines of fundamental disagreement” when it comes to defending strict liability over negligence and their competing rationales). 26. Safe Food Committee at p. 33, supra at Note 15. 27. C. Bruhn, Consumer Concerns: Motivating to Action, EID 3(4):511–515 (Oct-Dec 1997). 28. Madden and Owen on Products Liability, vol. 1, §5.2, 3d Ed. 2000.This rationale was the one most often emphasized by Chief Justice Traynor in those early cases holding in favor of strict product liability. Greenman v.Yuba Prods., Inc., 377 P.2d 897 (Cal. 1962); Escola v. Coca Cola Bottling Co., 150 P.2d 436, 440 (Cal. 1964) (Traynor, J., concurring); see also Roger W. Traynor, The Ways and Meanings of Defective Products and Strict Liability, 32 Tenn. L. Rev. 363 (1965). 29. Owen at p. 855, supra at Note 9. 30. 9 C.F.R. § 417.2(a)(1). 31. See Kriefall v. Excel Corp., 265 N.W.2d 476 (Wis. App. 2003) (arguing, ultimately unsuccessfully, that the USDA’s interpretation of the Federal Meat Inspection Act preempted state product liability law on what constitutes a defective meat product). 32. Golan at pp. iv–vi, supra at Note 4. 33. J.C. Buzby et al., Product Liability and Microbial Foodborne Illness, Economic Research Service/USDA,AER-799, at p. iv. 34. Safe Food Committee at p. 83, supra at Note 15. 35. FED.R.EVID. 407. 36. FED.R.EVID. 407,Advisory Committee Notes to 1972 Proposed Rules (citing Falknor, Extrinsic Policies Affecting Admissibility, 10 Rutgers L. Rev. 574, 590 (1956)). 37. The Jungle, 1906. 38. S.F. Alterkruse, M.L. Cohen and D.L. Swerdlow, Emerging Foodborne Diseases, EID, 3(3); 285–293. 39. Id.; see also S.R. Crutchfield, et al., An Economic Assessment of Food Safety Regulations: The New Approach to Meat and Poultry Inspection, ERS/AER No. 755, July

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50. 51. 52. 53. 54.

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1997. pp. 4–5. For the definition of the term “highly susceptible population” see 2001 FDA Food Code 1-201.10(B)(44). F.E. DeRuiter & J. Dwyer, Consumer Acceptance of Irradiated Food: Dawn of a New Era? Food Serv.Tech. 2(2), June 2002. Frenzen at pp. 2020–2026, supra Note 4. 69 Fed. Reg. 56,825 (Sept. 22, 2004). Green v. Smith & Nephew AHP, Inc., 629 N.W.2d 727 (Wis. 2001). See, generally Marshall Shapo, The Law of Product Liability, Vol. 2, Chap. 29, 3d ed. 1994. Owen, Punitive Damages in Products Liability Litigation, 74 Mich. L. Rev. 1257, 1278 (1976). Tauxe at pp. 518–519, supra Note 3; GAO Report at pp. 14–16, supra Note 2. Alterkruse at p. 288, supra Note 36. See also J. Buzby, Older Adults at Risk of Complications from Microbial Foodborne Illness, Food Review 25(2); 30–35. K. Ching, Jury Awards Hotel Guests $25 million for Illness, Reno Gazette Journal, May 20, 2002. See, e.g., Public Comment, FDA Docket No. 99F-5321, dated May 14, 2001, available online at www.centerforfoodsafety.org/pubs/CommentsFDARefrigeratedMeat5.14.2001. pdf.Well over one hundred groups are listed on the Public Citizen Web site as being opposed to irradiated food. Frenzen, supra at Note 4; Bruhn, supra at Note 26. M. Osterholm and M. Potter, Irradiation Pasteurization of Solid Foods: Taking Food Safety to the Next Level, EID, 3(4); 575–577. See, e.g. Tauxe at p. 516, supra at Note 3. Asbestos Litigation Costs and Compensation: An Interim Report, RAND Institute for Civil Justice (2002) available online at www.rand.org/publications/DB/DB397/. H.L.A. Hart,“Legal Responsibility and Excuses,” in Punishment and Responsibility 28, 44 (1968).

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

Chapter 17 TECHNICAL CHALLENGES AND RESEARCH DIRECTIONS IN ELECTRONIC FOOD PASTEURIZATION Suresh D. Pillai, Les Braby, and Joe Maxim

Introduction Foodborne diseases around the world are at unacceptable levels. Even five years ago, the data suggested that there were over 76 million cases of foodborne illnesses in the United States (Mead and others 1999). Many of these infections are preventable.They are preventable by improved food production methods, improved food processing methods, and improved food preparation and consumption practices within households (Pillai, 2004).The food industry has a number of “weapons” in its arsenal to prevent and destroy pathogens from food. Food irradiation technology is just one of many.Though this technology was patented 100 years ago in 1905 and thoroughly tested and validated over the past 50 years, unfortunately it is still one of the most maligned, misunderstood, and underutilized food processing technologies.The reasons for the confusion and lack of understanding of this technology are complex and have been discussed elsewhere in the book. Given the concerns associated with the transport, storage, occupational hazards, and disposal of cobalt-60 or cesium-137 isotope sources, we believe that electron beam/X-ray sources would be the food pasteurization technology of choice in both the developed and developing regions of the world.The fact that ionizing irradiation is the only technology known to be totally effective with frozen products in their final packaged form without discernable damage makes it an even more attractive technology.The term “electronic pasteurization” has been coined for the pasteurization achieved by electron beam and X-ray technologies.Though the use of electron beam as a pasteurization process has 279

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been thoroughly validated in a number of laboratories worldwide, there are still some lingering technical issues that limit its true applicability. These issues would become critical as the types of foods, packaging materials, pathogens of concern, and processing methods change or evolve in the future.The focus of this chapter is to highlight some of these technical challenges and potential research questions.The nontechnical force at play surrounding the widespread adoption of this technology by the food industry has been thoroughly discussed elsewhere and is not discussed in this chapter. This chapter provides a “road map” for those involved in research and development activities related to electronic pasteurization.

Target Pathogens Enteric Viruses Develop predictive model of virus inactivation as a function of dose, radiation quality, chemical properties of the environment, and virus surface characteristics. According to CDC estimates, viral pathogens account for more than 9 million cases, with Noroviruses being the key viral pathogen (Mead and others 1999). Noroviruses are of particular concern primarily because of their multiple routes of transmission (food, fomite, water, contact). The food processing and food service industries are particularly at risk given the potential for cross contamination.This virus is especially resistant to chlorination and other commonly used disinfectants.The recent outbreak of Hepatitis A associated with green onions in Pennsylvania (which resulted in more than 500 illnesses) is an example of how viral infections can result from contaminated fresh produce (CDC 2003). Unfortunately, very little information is available related to the irradiation kinetics of enteric viruses (Pillai 2004; Smith and Pillai 2004). Even though enteric viruses are resistant to ionizing radiation compared to enteric bacteria, recent reports from our laboratories suggest that enteric viruses are sensitive to electronic pasteurization at levels significantly lower than those produced with gamma radiation (cobalt-60) (Pillai and Espinosa 2003). Nevertheless, a concerted effort is needed to develop electronic pasteurization protocols that are effective at achieving viral inactivation while maintaining the sensory attributes of the foods. Developing electronic pasteurization protocols for Norovirus, for example, can be problematic at present because other than molecular methods, tissue culture methods

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for viral enumeration are nonexistent. It would be a technical challenge to validate inactivation kinetics for a pathogen when enumeration methods are unavailable.Though investigators have used Norovirus surrogates (for example, feline calicivirus [FCV] that can be enumerated) for disinfection and other studies (Goyal 2004), the surface characteristics of FCV are quite distinct from those of Noroviruses.These differences may be so significant that we may ultimately find that it was erroneous to extrapolate the findings. Given the vulnerability of vegetable produce to becoming contaminated with fecal sources during both pre- and post-harvest handling, it is essential that the inactivation kinetics of key viral pathogens such as Adenovirus, Rotavirus, Hepatitis A virus, Reovirus, and Astroviruses on fresh fruits and produce be delineated. Protozoan Pathogens Develop dose response relationships, oxygen enhancement ratios, and dose rate effectiveness data for all significant protozoan pathogens. Protozoa such as Cryptosporidium sp., Cyclospora sp., and Toxoplasma gondii are key pathogens that can be transmitted via foods. Even though the environmentally resistant stages of these organisms are larger than bacteria and are theoretically more sensitive to electronic pasteurization than bacterial cells, the inactivation kinetics of these organisms in minimally processed foods and ready-to-eat (RTE) foods are virtually unknown. Understanding the applicability of e-beam and X-ray technologies to inactivate these pathogens is essential. It is currently estimated that approximately 50% of all T. gondii infections in the United States happens through foods (Mead and others 1999). Bacterial Pathogens Measure dose response as a function of radiation quality and environmental factors, such as oxygen and radical scavenger concentrations, for Vibrio species and other bacteria that have not been fully characterized. Though there has been a significant amount of information related to use of ionizing radiation to inactivate bacterial pathogens such as Salmonella spp., Listeria spp., and E. coli O157:H7, the number of published reports dealing with V. vulnificus is still rather limited.This particular pathogen has a very high (40%) case fatality ratio (Mead and others 1999). There is a need for a better understanding of the inactivation kinetics of V. vulnificus in oysters. Such an understanding is particularly critical be-

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cause this pathogen is extremely lethal. It is estimated that approximately 50% of all Vibrio infections in humans occur via foods. Radiation Physics and Chemistry Chemical Environment Develop predictive model of the direct and indirect effects of ionizing radiation on viruses and cells as a function of radical scavenger mobility and reactivity, and of temperature, oxygen concentration, and other sources of radicals in the system. Electronic pasteurization is assumed to inactivate microorganisms by either direct damage or indirect damage to their nucleic acids. However, there are still lingering questions regarding the actual contribution of direct versus indirect damage to nucleic acids.The importance of indirect damage to nucleic acids is evident when one analyzes the inactivation of viruses. Studies in our laboratory and that of others have shown that viruses, although very small, are quite sensitive to e-beam irradiation. Studies in our laboratory using Poliovirus type 1 in different matrices have shown that the D10 value ranges between 1.83 and 2.82 depending on the matrix (Pillai and Espinosa 2003). Peptone was found to shield the viruses from rapid inactivation.These studies were conducted using suspensions containing approximately 10,000 virus particles per milliliter, which in reality is a relatively small number of targets for direct attacks. The “shielding effects” or “scavenger activity” exhibited by peptone suggests that in some situations, the indirect effects of irradiation may be the primary mode of action. This possibility, however, needs to be further studied and verified.Additional research to delineate the precise mechanisms of irradiation-induced inactivation is needed because this can allow the incorporation of specific “quenching” molecules directly to the food, the matrix, or into the packaging materials to attain or prevent a certain desired level of nucleic acid damage.This can be particularly important when attempting to develop low-dose irradiation protocols on multicomponent foods that may contain these scavenger molecules that may inadvertently reduce the desired effect. Standardized Protocols Develop and validate standardized protocols for measuring pathogen survival, characterizing dose uniformity, and evaluating sensory and nutritional effects.

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There is a strong need for standardized protocols for evaluating the effectiveness of electronic pasteurization on emerging pathogen destruction in pure culture and in samples. Given the anticipated increase in the emerging pathogen list, poorly designed studies coupled with erroneous dose measurements can be a significant detriment to the field. Federal agencies such as the U.S. EPA have developed standardized protocols for evaluating the claims of point of use (POU) filtration devices. Similar protocols should be developed by the USDA or the FDA for identifying the inactivation kinetics of foodborne and water-borne pathogens.The availability of standardized protocols would assist the food industry in developing specific irradiation protocols that are applicable to their specific needs. Very often it is a specific commercial entity that has the resources to develop electronic pasteurization protocols for specific food items. For example, different companies may have commercial interest in the use of e-beam to inactivate viral pathogens in fruit juices, fruit pulp, on fruit surfaces, and so on.Thus, without standardized protocols there is a potential for technical errors in experimental design and data interpretation.The use of standardized protocols would definitely aid in data validity and comparison of results from multiple laboratories. Coupled with standardized ISO/ASTM standards and protocols for delivering and measuring dose, standardized protocols should also be developed for sensory and other attributes.The ISO/ASTM Standards on Nuclear Technology and Applications were created and maintained by Committee E10, formed in 1951 and having a current membership of approximately 250 members, including representatives from more than 20 countries.The E10 Committee has jurisdiction of over 104 standards.These standards continue to play a preeminent role in all aspects important to the irradiation industry, including standardization of irradiation dosimetry, package systems, and materials.The use of multidimensional gas chromatography for analytical determination of the formation of specific odoriferous compounds in irradiated foods should be explored (Pillai 2004).Without such standardization it would be impossible to compare and analyze electronic pasteurization results for multiple pathogens, multiple foods, and from multiple laboratories. Electronic Pasteurization in Conjunction with Microbial Risk Assessment Develop formalism for determining the appropriate level of microbe inactivation as a component of a HACCP plan. Current electronic pasteurization practices are based on the 6-log reduction of the target organism.There is no doubt that the 6-log reduction

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provides for an adequate safety margin for products such as ground beef and fresh/frozen poultry. However, the applicability of using a 6-log reduction process for pathogens that are usually at low levels in ready-toeat foods, and in minimally processed foods (for example, fresh produce) is debatable. Electronic pasteurization was never meant to be a standalone process. Electronic pasteurization should be used only as an integral step in a HACCP plan. Using this food processing technology to avoid currently employed disinfection and intervention strategies would be disastrous and detrimental to the technology. Certain commodities such as fresh produce and some RTE foods undergo undesirable sensory changes during such pasteurization processes. Quantitative microbial risk-reduction studies should be conducted to evaluate the possibility of targeting only a 1-to-2-log reduction of key viral and bacterial pathogens on specific foodstuffs.These studies could lead to significant cost reduction (due to reduced time under e-beam or X-ray) as a result of reduced dose. It can be argued that because electronic pasteurization is theoretically the last critical control point, employing 6-log reduction at this final step may be overkill.The use of low-dose electronic pasteurization protocols can also help preserve the sensory attributes of the food in question. Low Dose Electronic Pasteurization and Dosimetry Develop methods for optimizing facility design in terms of throughput, capital cost, and operating cost for products requiring different values of dose and dose uniformity. Methods for setting accelerator current to lower values in order to achieve lower e-beam dose rates in the conventional belt speed range need to be explored.The minimum current that can be achieved by typical linear accelerators should also be determined. Because capital cost of the facility is a major consideration in terms of cost of electronic pasteurization processing, a study of the net cost of processing using beam current reduction and X-ray pasteurization should be conducted. If X-ray pasteurization is significantly more efficient when low doses are required, the relative biological effectiveness of X-rays relative to electrons for bacterial inactivation and other relevant endpoints must be determined. Improved dosimeters, more sensitive and reproducible radiochromic film, an increase in the sensitivity of ESR measurements, or a variation of thermo luminescent dosimetry that could measure radiation doses in the range of 10 Gy to 1000 Gy will be needed as the range of products and the objectives of electronic pasteurization expand.A dosimeter certification service, similar to that currently existing for radiation protection

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dosimeters, will be needed to assure consistent results at different processing and research facilities. Having this service will require development of standardized techniques for placing dosimeters and also development of standard methods for reading dosimeters (Braby 2003)

Product Packaging Explore packaging options to maximize microbial control and minimize impact on product quality. The packaging material industry will find greater involvement in electronic pasteurization research.There is a need to prevent adverse sensory changes during electronic pasteurization combined with the possibility of incorporating antimicrobial components in packaging materials. Studies suggest that modified atmosphere packaging (MAP) in combination with electronic pasteurization can improve the chemical, physical, and microbiological safety of a variety of foods (Song and others 2003; Fan and others 2002; Fan and others 2003). Research on synergistic action by antimicrobial coatings/antioxidant additions and electronic pasteurization can provide avenues that could potentially extend the product lines for which electronic pasteurization becomes a viable option. The development of “intelligent” packaging material or indicators that can visually denote an electronically pasteurized product, or dose range, or detect adverse changes in a product can also find commercial application. The ASTM Subcommittee E10.06 was organized to create and formalize ISO/ASTM standards for package systems.

Electronic Pasteurization of Complex-Shaped Packages Optimize dose measurement and display to improve understanding of effect of package configuration on dose uniformity and product quality. Develop option for dynamic control of beam energy and/or intensity to deliver specified doses to different parts of a packaged product. Accurate dose mapping and dosimetry of complex-shaped packages will become a necessity in the future as RTE foods and other variably shaped food items are approved for electronic pasteurization.As the need for more intricate dose allocation arises, more and more sophisticated dose delivery techniques need to be developed. Research is needed to identify the specific dose needs in the high and low zones of a specific

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complex geometry and create the appropriate dose delivery scheme(s) to accomplish these goals. The use of computer visualizations or simulations to determine dose distribution in an irregularly shaped object can be a valuable tool. If RTE foods cannot be packaged in a way that results in optimum dose to each component using a uniform incident beam, the desired doses can be achieved by using intensity modulated beams. In recent years intensity modulation has become routine in radiation therapy, and similar techniques using automatically controlled beam collimators, variable energy attenuators, or active control of beam scan rates could be used to deliver different doses to specified parts of a package. Active monitoring of the position of the product would be required, and throughput may be reduced, but this level of control may be warranted for high-value products. Further research is needed regarding orientation of complex package shapes so that the cumulative dose will meet the target minimum at any point in the target mass, yet the cumulative maximum dose will be below the mandated maximum allowable. Finally, major advancements in electronic pasteurization can be possible when there are stronger collaborations between researchers involved in product formulation, product packaging, microbiology, dosimetry, and marketing.

Acknowledgements This work was supported in part by the USDA-CSREES Special Grant 2004-06077 and USDA-CSREES/IFAFS grant 00-52102-9637.

References Braby LA. 2003. The underlying principles of E-beam technology. Annual Meetings of the Institute of Food Technologists. Chicago. June. [CDC] Centers for Disease Control and Prevention. 2003. Hepatitis A outbreak associated with green onions at a restaurant. Monaca, Pennsylvania, 2003, Dispatch 52:1–3. Fan X, Sokorai KJ. 2002. Changes in volatile compounds of gamma-irradiated fresh cilantro leaves during cold storage. J Agric Food Chem 50:7622–7626. Fan X,Toivonen PM, Rajkowski KT, Sokorai KJ. 2003.Warm water treatment in combination with modified atmosphere packaging reduces undesirable effects of irradiation on the quality of fresh-cut iceberg lettuce. J Agric Food Chem 51:1231–1236. Goyal SM. 2004. Viruses in Food. In: Bier RC, Pillai SD, Phillips TD, Ziprin RL, editors, Preharvest and Postharvest Food Safety. Chicago:IFT Press, Blackwell Publishing, p. 101–119.

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Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, Griffin PM, Tauxe RV. 1999. Food-related illness and death in the United States. Emerg Infect Dis 5(5):607–625. Pillai SD. 2004. Food Irradiation. In: Bier RC, Pillai SD, Phillips TD, Ziprin RL, editors, Preharvest and Postharvest Food Safety: Contemporary Issues and Future Directions. Chicago:IFT Press, Blackwell Publishing, p. 375–387. Pillai SD, Espinosa IY. 2003. E-beam inactivation of RNA and DNA containing viruses. Abstract. Annual Meetings of the American Society for Microbiology. Washington, D.C. May. Smith S, Pillai SD. 2004. Irradiation and food safety: scientific status summary. Food Technol 58:48–55. Song IH, Kim WJ, Jo C,Ahn HJ, Kim JH, Byun MW. 2003. Effect of modified atmosphere packaging and irradiation in combination on content of nitrosamines in cooked pork sausage. J Food Prot 66:1090–1094.

Food Irradiation: Research and Technology Edited by Christopher H. Sommers, Xuetong Fan Copyright © Blackwell Publishing and the Institute of Food Technologists 2006

INDEX

Active control of beam scan rates, 286 Acyl-oxy bond, 47 Additives combination of, with irradiation, 188–190 in control of off-odor production and color changes, 137–138 definition of, 37 and packaging combinations, 138–139 radiation and, 38 ready-to-eat products and, 139 Adenovirus, 281 Adult stage of insects, tolerance to irradiation and, 145–148 Aerobic packaging, 134–135, 139 Aerobic Plate Count (APC), 98 Aflatoxins, 221, 222–224, 227–228 Agarose gel electrophoresis, 93–94 Agmatine, 254 Agreement on the Application of Sanitary and Phytosanitary Measures, 159 Agricultural commodities, globalization of trade in, 68 Agricultural Marketing Service (AMS), 237, 240, 246 Agricultural practices, good, 224–225 Agriculture Department of. See U.S. Department of Agriculture (USDA) State Department of, 237 Alanine, 112

Absorbed dose, 106 versus beam current, 21 definition of, 12–13, 107 dosimetry and, 107 versus emitted radiation power, 12–13 maximum, 106 minimum, 106 Absorbed dose distribution, 113–114 Absorbed dose mapping, 113 ac. See Alternating current (ac) 2-ACBs. See 2-Alkylcyclobutanones (2-ACBs) Acceleration tubes, 22 Accelerator facility, 117, 118, 119 Accelerator irradiator, 118 Accelerators Cockcroft-Walton, 23 constant-potential, 22–24, 25 Dynamitron, 23–24 electron beam, 21–28 Electron Transformer-Rectifier, 23 microwave linear, 24–26 radio-frequency, 26–28 Rhodotron, 26 Accidental post-irradiation dosimetry, 89 Acetic acid, 190–191 Achromobacter, 223 Acid-adapted organisms, 187, 191 Acidification, shelf-life and, 175 Acids, lipid peroxidation and, 229 Acrylamide, 43, 51

289

290

Index

Alanine dosimeters, 108–109 Albumen loss of, in eggs, 201–202 total protein content of eggs and, 203 Albuminuous sac, irradiation-induced rupture of, in eggs, 201–202 Alcohol, formation of tumors and, 43 Aldehydes, 131, 138, 139 branched-chain, 133 lipid peroxidation and, 229 volative, 137 2-Alkylcyclobutanones (2-ACBs), 40, 46, 47–49, 50, 51, 52, 54, 55, 85, 95–96 chromatogram of, 97, 99 in detection of prior irradiation treatment of eggs, 216 formation and levels of, in foods, 46–51 genotoxicity of, 52 radiation-induced formation of, from precursor fatty acids, 48, 49–50 toxological safety of, 52–54 tumor promotion and, 54–55 Allergies egg, 216 food, reduction of, by ionizing radiation, 250, 251 latex, 272 Almond Board of California, 224, 225–226 ALTA 2341 preservatives, 193 Alternating current (ac), 22 Alternative treatment efficacy approach, 151, 152 Aluminum, 118 American Council on Science and Health, 73 American Dietetic Association, 240 American Legal Institute’s Third Restatement of the Law,Torts: Products Liabillity, 79–80 American Medical Association, 240 American National Cattlewomen, 77 American Society for Testing and Materials, International (ASTM), 106, 285 Amines, 45 biogenic, 46, 252–254

Amino acid radiolysis, 133 Amino acids in eggs, 209 sulfur, 133 Amino acid side chains, 133, 134 AMS. See Agricultural Marketing Service (AMS) Animal and Plant Health Inspection Service (APHIS), 6, 152–153, 154, 156–157, 158, 160 Animals, toxocological research using, 44–45 Antibrowning agents, 178 Anti-irradiation campaign, 70 Antioxidants, 137, 138–139 increased capacity of, 178 increase in activity of, 255–256 lipid oxidation and, 139 lipid peroxidation and, 230 phytic acid and, 255 radiation resistance and, 180 radiation tolerance and, 215 Anti-Stokes property, 90–91 APC. See Aerobic Plate Count (APC) APHIS. See Animal and Plant Health Inspection Service (APHIS) Apple juice formaldehyde and, 46 furan and, 40 “Application of Irradiation to Phytosanitary Problems,” 158, 159 APPPC. See Asia and Pacific Plant Protection Organization (APPPC) Aqueous carbohydrate solutions, pure, radiolysis of, 92–93 Area processing coefficient (K(x)), 21 Arthropods, 144, 145, 153, 156 Artificial inoculation of insects, 148 Asbestos, 274–275 Ascorbate, 137 Ascorbic acid, 137, 138 combination of, with irradiation, 190 effect of, on color and off-odor, 139 phytic acid and, 255 sensitivity of, to irradiation, 177 Asia and Pacific Plant Protection Organization (APPPC), 159 Asparagine, 136

Index Aspergillus flavus, 222, 227 Aspergillus parasiticus, 222, 227, 228 Asthaxanthin, 191–192 ASTM. See American Society for Testing and Materials, International (ASTM) Astroviruses, 281 Atomic Energy of Canada Ltd., 26 Attenuators, variable energy, 286 Australia, 7, 153 Automatically controlled beam collimators, 286 a* values, color, 135, 137, 138 Azoxymethane, 54–55 BA. See Biogenic amine (BA) Bacillus, 130, 223 Bacillus cereus nuts and, 228 school illness and, 239 Bacteria enteric, 280 internalization of, 172 lactic acid–producing, 257 planktonic, 173 research and, 281–282 resistance of, to radiation, 171, 280 spoilage, D-values of, 130 Bacterial biofilms, 172 Bacteriological modifications, 98 Bait and switch tactic, use of term cold pasteurization and, 274 Batch homogeneity, dosimetry and, 111 Beam electron. See Electron beam (e-beam) intensity modulated, 286 Beam collimators, automatically controlled, 286 Beam current, absorbed dose versus, 21 Beam divergence, Rhodotron beam scanners and, 28 Beam energy, accelerator facility and, 118 Beam scan rates, active control of, 286 Beam spot profile, accelerator facility and, 118 Becquerel (Bq), 15

291

Beef, ground, irradiated. See Irradiated ground beef Beef fat, oxidized, colon cancer and, 55 Benefits versus risks, 64, 66 Benzene, 43, 45, 54 BHA. See Butylated hydroxyl anisol (BHA) Bias, dosimetry and, 111 Biofilms, 172–173 Biogenic amine (BA), 46, 252–254 Bird seed, 161–163 Bones, dating, ESR signal measurement in, 89 Botulin toxin, 73 Botulism, risk for, 193–194 Bq. See Becquerel (Bq) Branched-chain aldehydes, 133 Brand names, consumer trust in, 265 Brazil, 7 Bremsstrahlung, 29, 111 Brevibacterium, 223 Bronchothrix, 193 Brown discoloration in irradiated raw red meat, 134 Budker Institute of Nuclear Physics, 23, 26–27 Bureau of Chemical Safety, 45 Butylated hydroxyl anisol (BHA), 255 CaA. See Calcium ascorbate (CaA) Cadaverine, 254 Calcium phytic acid and, 255 produce and, 179–180 rradiation and, 179–180 Calcium ascorbate (CaA) combination of, with irradiation, 179–180 produce and, 180 Calcium chloride, 180 Calcium lactate, 180 California Supreme Court, 265 Calorimeters, 108–109 Campylobacter, 69 Campylobacter jejuni, 130 eggs and, 201 nuts and, 228

292

Index

Cancer, incidence of, consumption of fruits and vegetables and, 178 Canned tongue, 265 Capacitive systems, constant-potential accelerators and, 23, 24 Capital cost, low-dose electronic pasteurization and dosimetry and, 284–285 Capital investment in dosimeter, 110 Capric acid, 48 Carbohydrates formaldehyde and, 45–46 furan and, 39–40 radiolytic products from, in detection of irradiated foods, 92–93 Carbohydrate solutions, pure aqueous, radiolysis of, 92–93 Carbon dioxide, 225 Carbon monoxide-myoglobin (CO-Mb), 136–137 Carbonyls, 132 Carcinogens, 40, 43 Carotenoids in egg yolk, 207 oxidation of, in eggs, 203 Carrier, irradiator dose mapping and, 115 Cascaded rectifier systems, constantpotential accelerators and, 22 Cattle Buyers Weekly, 66 Cattlemen’s Beef Board (CBB), 70 CBB. See Cattlemen’s Beef Board (CBB) CDC. See Centers for Disease Control and Prevention (CDC) Cellular leakage, 176 Cellular wall modification, gas evolution and, 97 Cellulose, crystalline, ESR measurement and, 89 CEN. See European Committee for Standardization (CEN) Center for Food Safety, 273 Centers for Disease Control and Prevention (CDC), 68, 240, 263, 280 FoodNet Population Survey of, 71 school illness and, 239 Ceric-cerous dosimeters, 108–109

Certification dosimeter, 284–285 product, dosimetry and, 123–124 Certified raw milk, 63 Cesium-137 (Cs-137), 14, 279 cfu. See Colony-forming unit (cfu) Characterization of dosimetry facility, 115, 117–118 Chemical changes of irradiated seafood, 191–192 Chemical environment, radiation physics and chemistry and, 282 Chemiluminescence, 91 Chemistry, radiation, 282–285 Chicken, whole, dose mapping of, 119 Chicken eggs. See Eggs Chief of Food and Agro-Industries, FAO, Rome, Italy, 68 Children, effect of, on consumer acceptance, 75 Chlorination, 63, 81 combination of, with irradiation, 178–179 risks versus benefits of, 66 shelf-life and, 175 Chlorine, biofilms and, 172 Chlorine wash, pathogen regrowth and, 173 Chlorophyll breakdown, irradiation and, 249, 256 Cholesterol colon cancer and, 55–56 microcidal effect and, 129 Cholic acid, colon cancer and, 55–56 Chromatography of 2-alkylcyclobutanones, 97, 99 gas, volatile hydrocarbons and, 94–95, 96 silver, 99 of volatile food extracts, 92 Circe S-band systems, 25–26 Cis 2-tetradec-5’-enyl-cyclobutanone ratio, 95 Citrate, 137 Citric acid, 190–191 Clean Air Act, 225 Clostridium, 130 Clostridium botulinum, 193, 228

Index Clostridium perfringens nuts and, 228 school illness and, 239 seafood and, 185 Co-59. See Cobalt-59 (Co-59) Co-60. See Cobalt-60 (Co-60) Cobalt-59 (Co-59), 14 Cobalt-60 (Co-60), 14–15, 129, 279, 280 Cockcroft-Walton accelerators, 23 Codex Alimentarius, 7, 86, 155 Codex General Standard for Irradiated Food, 155 Codex Recommended International Code of Practice for the Operation of Irradiation Facilities, 155 Codling moth larvae, 150 Cold pasteurization, 64, 274 Cold smoking, 186 Cold storage warehouses, 8 Coleoptera, 144 Coliforms, 223, 224 Collimators, automatically controlled beam, 286 Colony-forming unit (cfu), 172 Color change in, in irradiated meat, 127–128, 134–137 improvement in, of plant extracts, 256–257 Colorado Boxed Beef, 79 24-Color-Fluorescence-In-SituHybridization, 54 Columbus, Christopher, 64 CO-Mb. See Carbon monoxidemyoglobin (CO-Mb) Comet Assay, 52, 54 Comite de Sanidad Vegetal del Cono Sur (COSAVE), 159 Commercial facility, dosimetry at, 114–124 Committee E10, 283 Commodies, fresh horticultural. See Phytosanitary treatment for fresh horticultural commodities, irradiation as Community Bureau of Reference, 85 Competing microflora, irradiation processing and, 191–192

293

Complex-shaped packaging, 285–286 Compton electrons, 128 Conalbumin, 203 Constant-potential accelerators, 22–24, 25 Consumer acceptance and marketing of irradiated foods, 63–84 barriers to acceptance of, 75–76 children influencing, 75 counteraction of unfavorable information and, 73–74 defining moment in food safety and, 79–80 education as key to, 70–72 effect of unfavorable information on, 72–73 farm to fork and, 80 gender influencing, 75 income influencing, 75 irradiation as powerful tool to improve food safety and, 67–68, 69 legal actions and, 80 marketing of irradiated ground beef and, 78–79 Minnesota Model of consumer acceptance and, 76–78 resistance to new technology and, 64, 65 risks versus benefits and, 66 safety of food supply and, 66–67 Continuous wave (CW) mode, 28 Contract service irradiators, 8 Cooked meat, color changes in, by irradiation, 134–135 COSAVE. See Comite de Sanidad Vegetal del Cono Sur (COSAVE) Counteraction of unfavorable information, consumer acceptance and, 73–74 Coupling methods, constant-potential accelerators and, 22–23 Covariance analysis, insect irradiation studies and, 149 Cryptosporidium, 281 Crystalline cellulose, ESR measurement and, 89 Crystalline sugars, 89 Cs-137. See Cesium-137 (Cs-137)

294

Index

Curculionid pests, 154, 158 Curie, Marie, 78 Cut flowers, phytosanitary treatments for, 161–163 CW mode. See Continuous wave (CW) mode Cyclobutanone, 2-ACBs and, 48 Cyclohexanone, 53–54 Cyclospora, 281 Cysteine, 133 D10 values. See also D-values of foodborne pathogens and spoilage bacteria, 130, 175 fungi, viruses, and bacteria and, 171 Listeria monocytogenes and, 188–189 Staphyloccus aureus and, 188–189 starvation of exponential phase cells and, 191 Damages, punitive, negligence and, 272–273 dc. See Direct current (dc) 2-DCB, 54 2-dDCB. See 2-Dodecylcyclobutanone (2-dDCB) Defective food product liability for manufacture of, 264–267 proving existence of, 266–267 Defects, liability and, 266 DEFT. See Direct Epifluorescence Filter Technique (DEFT) DEFT/APC. See Direct Epifluorescence Filter Technique/Aerobic Plate Count (DEFT/APC) DeGregori,Thomas R., 64, 66 Dehydroascorbic acid, 177 Department of Agriculture. See U.S. Department of Agriculture (USDA) of Health and Human Services, 40, 240 State of Agriculture, 237 of Education, 237 Depth, half-value, as range parameter, 118 Depth-dose distribution, accelerator facility and, 118, 119 Design defects, liability and, 266

Detectable light, luminescence and, 89–90 Detection of irradiated foods, 85–104 analysis of stable radiolytic products and, 91–96 free radicals and electronic excited states and, 86–91 irradiated ingredients and low-dose irradiated plants and, 98–99 modification of macroscopic physico-biological parameters of food and, 96–98 Diapausing strains of insects, 148 Diaspidid scale insects, 145, 148 Dichloromethane, volatile Nnitrosamines dissolved in, 252 Dichromate dosimeters, 108–109 Diet, tumor promotion and, 55–56 Dihydrothymidine, 93 Dimerization, free radicals and, 128–129 Dimethyl disulfide, 132, 231 Dimethyl sulfide, 132, 231 Dimethyl trisulfide, 132, 231 DinD gene, 53 Dipalmitoyl-phosphatidyl-ethanolamine, 47 1,1-Diphenyl-2-picrylhydrazyl (DPPH), 255 Diptera, 144 Direct current (dc), 22 Direct Epifluorescence Filter Technique/ Aerobic Plate Count (DEFT/APC), 86 Direct Epifluorescence Filter Technique (DEFT), 98 Disinfestation, insect. See Insect disinfestation Disinfestation track, 6–7 Disproportionation, free radicals and, 128–129 Dissociation, irradiation and, 128 Distribution centers, contract service irradiators in, 8 Dmax. See Maximum absorbed dose (Dmax) Dmin. See Minimum absorbed dose (Dmin)

Index DNA, 93 microcidal effect and, 129 repair of, 130 Documentation, product release and certification and, 123–124 2-Dodecylcyclobutane, 240 2-Dodecylcyclobutanone (2-dDCB), 47, 49, 52–53, 54, 55, 95 Dose absorbed. See Absorbed dose gamma-ray facility and, 117–118 target, 121 versus temperature rise, 13–14 to water, 107 Dose distribution, 13 Dose limits, 105, 121 Dose mapping, 113 absorbed, 113 dose distribution and, 13 dosimetry and, 110 irradiator, 115–117 product, 119–120 Dose rate, gamma-ray facility and, 117–118 Dose response tests, insect irradiation studies and, 149 Dose uniformity ratio (DUR), 18, 116–117, 120, 149 Dose uniformity rule (DUR), 29–30 Dosimeter certification service, 284–285 Dosimeters, 107 alanine, 108–109 ceric-cerous, 108–109 definition of, 107 dichromate, 108–109 ease of use of, 110 ethanol-chlorobenzene, 108–109 Fricke, 108–109 post-irradiation change in response of, 109–110 primary-standard, 107–109 radiochromic, 109 reference-standard, 108–109 routine, 108–109 ruggedness of, 110 selection of, 109–111 thin film, 116

295

transfer-standard, 108–109 working, 108–109 Dosimetry, 105–126 accidental post-irradiation, 89 at commercial facilities, 114–124 in food research, 112–114 fundamentals of, 107 importance of, 105–106 insect irradiation studies and, 149 low-dose electronic pasteurization and, 284–285 radiation, 90 routine product, 122–123 selection and characterization of system of, 107–112 suitable dose range for application of, 109, 110 thermo luminescent, 284–285 types of systems of, 107–109 use of system of, 112 Double packaging, 134–135, 138–139 DPPH. See 1,1-Diphenyl-2-picrylhydrazyl (DPPH) Dried egg ionizing radiated. See Ionizing radiated dried egg microbial lethal effect of ionizing radiation in, 208 Dry foods, irradiated, rehydration of, 91 DUR. See Dose uniformity ratio (DUR); Dose uniformity rule (DUR) D-values. See also D10 values of foodborne pathogens and spoilage bacteria, 130, 175 fungi, viruses, and bacteria and, 171 Salmonella and, 229 Dynamitron accelerators, 23–24 E. coli. See Escherichia coli E. coli TRP Assay, 53 EB accelerators. See Electron beam (EB) accelerators e-beam. See Electron beam (e-beam) E-Beam X-Ray Solutions, 24 EBI. See Electron beam irradiator (EBI) ECB dosimeters. See Ethanol-chlorobenzene (ECB) dosimeters Ecology, phytoplane microbial, 171

296

Index

Economic Research Service, 268 EDB. See Ethylene dibromide (EDB) Education as key to consumer acceptance, 70–72 State Department of, 237 Egg powder, 209 Eggs allergies to, 216 classification of, 201–203 color changes in, caused by ionizing radiation, 202–203 dried. See Dried egg emulsifying qualities of, 199, 204, 207, 209 foaming qualities of, 199, 204, 209 frozen. See Frozen egg gelling qualities of, 199, 204, 209 grades of, 201–203 ionizing radiation of, 199–220 dried egg and, 208–210 frozen egg and, 210–211, 212–213, 214 future research in, 216 refrigerated liquid egg and, 204–208 shell-eggs and, 200–204 strategies to increase quality of irradiated egg products and, 215–216 liquid, refrigerated, 204–208 liquid whole. See Liquid whole egg (LWE) safe handling of, 271 Egg shell, 199. See also Shell-eggs Eggshell plaintiff rule, liability and, 271–272 Egg white ionizing radiated. See Ionizing radiated egg white liquid, ionizing radiation of, 206–207 microbial lethal effect of ionizing radiation in, 206 Egg yolk ionizing radiated. See Ionizing radiated egg yolk liquid, 207–208 Electrolyte leakage, irradiation and, 176

Electromagnetic microwave, 86–88 Electron beam (EB) accelerators, 21–28 Electron beam (e-beam), 129 advances in, for food technology. See Gamma ray, electron beam, and X-ray technologies, advances in, for food irradiation combination of, with chlorination, 178–179 mean energy of, accelerator facility and, 118 pathogen regrowth and, 173 produce and, 170, 173 technology and, 21–28 Electron beam facilities, 19–28 Electron beam irradiator (EBI), 201 Electron capture, free radicals and, 128–129 Electron facilities, 120 Electronic excited states, 91–96 detection of irradiated foods and, 86–91 luminescence and, 89–90 Electronic pasteurization, 279-280. See also Food irradiation; Irradiated foods low-dose, dosimetry and, 284–285 microbial risk assessment and, 283–284 Electron penetration in water, 20 Electron Processing Systems (EPS), 23 Electrons, Compton, 128 Electron spin resonance spectroscopy (ESR), 85, 86, 88, 89, 93, 216 Electron Transformer-Rectifier (ELV) accelerators, 23 Electrophoresis, agarose gel, mitochondrial DNA and, 93–94 ELV accelerators. See Electron Transformer-Rectifier (ELV) accelerators Emitted radiation power, absorbed dose versus, 12–13 Emulsifying qualities of eggs, 199, 204, 207, 209 Enteric bacteria, resistance of, to ionizing radiation, 280

Index Enteric viruses irradiation kinetics of, 280 research and, 280–281 Enteriditis, 224 Enterobacteriaceae, 210 Environment, chemical, radiation physics and chemistry and, 282 Environmental Protection Agency (EPA), 155, 283 Enzymatic hydrolysis, 99 EPA. See Environmental Protection Agency (EPA) EPPO. See European and Mediterranean Plant Protection Organization (EPPO) EPS. See Electron Processing Systems (EPS) Escherichia coli, 4, 5, 66, 130, 281 biofilms and, 172 combination of chlorination with irradiation and, 178 D10 values for, 174–175 5-fluorouracil and, 53 foodborne illnesses in children and, 238 frozen whole egg and, 210 in ground beef, 67, 241 lawsuits and, 80 manufacturing defects and, 267 nuts and, 223, 224, 228, 231 prevention of, by food irradiation, 69 reduction in, 68 school illness and, 239 treatment parameters for, 173 ESR. See Electron spin resonance spectroscopy (ESR) ESR spectroscopy, free radicals and, 86–89 Esters gallic, 137 lipid peroxidation and, 229 methyl and propyl, of parahydroxybenzoic acid, 190 Ethanol, 54 2-ACBs and, 55 volatile N-nitrosamines dissolved in, 252

297

Ethanol-chlorobenzene (ECB) dosimeters, 108–109 Ethylene dibromide (EDB), 155 Eugenol, 129 Eukaryotic cells, 54 European and Mediterranean Plant Protection Organization (EPPO), 159 European Commission, 156 European Committee for Standardization (CEN), 85, 86, 87, 90–91, 94, 99, 106 European Directive 1999/2/EC, 98–99 Excitation infrared pulsed laser beam, 90–91 irradiation and, 128 Excited states, electronic. See Electronic excited states Exemplary damages, negligence and, 272–273 Exopolysaccharide matrix, biofilms and, 172 Exponential phase cells, starvation of, 191 FAO, 68, 249 Farm Bill, 239–240 Farming, nut processing and, 222 Farm Security and Rural Investment Act of 2002, 239–240 Farm Service Agency (FSA), 237 Farm to fork, 68, 80 FASEB, 51 Fat, beef, oxidized, colon cancer and, 55 Fatty acids, 133 precursor, radiation-induced formation of 2-ACBs from, 48, 49–50 radiolysis of, 94 FCV. See Feline calicivirus (FCV) FDA. See Food and Drug Administration (FDA) FDA Food Code, 270–271 FDA/FSIS, 67 FDA Model Food, 271 Federal Food, Drug, and Cosmetic Act, 37–38 Federal Register, 154

298

Index

Federation of American Societies for Experimental Biology, 45 Feline calicivirus (FCV), 281 Female insects, tolerance of, to irradiation, 148 Fermented foods gamma irradiation and, 258 irradiation and, 257–258 Korean, 254, 257 Ferric myoglobin, 138 Ferric reducing antioxidant power (FRAP), 255–256 Ferricytochrome, 136 Ferrocytochrome, 136 Fish. See also Seafood electric impedance of, 97 irradiation as effective postprocessing treatment for, 187–191 low-fat, effect of irradiation on, 187 smoked, 186, 194 Flat earth theory, 64 Flavandiols, 256–257 Flavanoids, 256–257 Flavanols, 256–257 Flies, 152 Florisil, 96 Flowers, cut, phytosanitary treatments for, 161–163 Fluorescence, microscopic, 98 Fluorescence analysis of thymine glycol, 93 5-Fluorouracil (5-FU), 53 FNS. See Food and Nutrition Service (FNS) Foaming quality of eggs, 199, 204, 209 Food authorized or treated with irradiation, 161–163 defective. See Defective food product and Drug Administration (FDA), 14, 29, 37, 38, 44, 127, 154, 156, 227, 283 fermented, 257–258 formation and levels of 2-ACBs in, 46–51 globalization of trade in, 68

irradiated. See Food irradiation; Irradiated foods and Nutrition Service (FNS), 237 & Water, Inc., 73, 74 Food additives. See Additives Food Additives Amendment of 1958, 37 Food Advisory Committee, 40 Food allergies. See Allergies Foodborne illnesses produce-associated, 169 in school, 238–239 Foodborne pathogens, D-values of, 130 Food Code, FDA, 270–271 Food extracts, volatile, chromatograms of, 92 Food irradiation, 3-10, 128-129. See also Irradiated foods advances in gamma ray, electron beam, and X-ray technologies for, 11–36 consumer acceptance and marketing of irradiated foods and, 63–84 detection of irradiated foods and, 85–104 difficulties in adoption of, 7–8 dosimetry for food processing and research applications and, 105–126 driving forces for adoption of, 4–7 ionizing radiation of eggs and, 199–220 irradiated ground beef for National School Lunch Program and, 237–248 irradiation as phytosanitary treatment for fresh horticultural commodities and, 143–168 irradiation of seafood with particular emphasis on Listeria monocytogenes in ready-to-eat products and, 185–198 irradiation treatment of nuts and, 221–236 from legal perspective, 263–278 low, medium, and high dose ranges of, for food processing and research, 108

Index low dose irradiation of fresh and fresh-cut produce and, 169–184 mechanisms and prevention of quality changes in meat by irradiation and, 127–142 potential annual public health benefits of, 69 potential applications of ionizing radiation and, 249–262 regulation of irradiated foods and packaging and, 37–42 technical challenges and research directions in electronic food pasteurization and, 279–287 toxicological safety of irradiated foods and, 43–62 Food Irradiation Coalition/NFPA, 39 Food Irradiation Committee FoodNet Population Survey, 71 Food processing, dosimetry for. See Dosimetry Food research, dosimetry in, 112–114 Food safety defining moment in, 79–80 and Inspection Service of U.S. Department of Agriculture, 66–67 irradiation as tool to improve, 67–68, 69 Food safety track, 4–6 Formaldehyde, 43, 45–46, 54 Formosa, 154 Forward mutagenesis assays, 53 Frame-shift mutations, 43 Framework Equivalency Work Plans, 158, 160 FRAP. See Ferric reducing antioxidant power (FRAP) Frass, nuts and, 222, 227 Free radicals, 85, 91–96, 128–129, 133, 282 amino acid side chains and, 134 detection of irradiated foods and, 86–91 frozen meat and, 131 lipid peroxidation and, 229 nuts and, 231 Free radical terminators, 137

299

Fresh-cut produce, low dose irradiation of. See Low-dose irradiation of fresh and fresh-cut produce Fresh horticultural commodies, irradiation as phytosanitary treatment for. See Phytosanitary treatment for fresh horticultural commodities, irradiation as Fresh produce, low dose irradiation of. See Low-dose irradiation of fresh and fresh-cut produce Fricke dosimeters, 108–109 Frozen egg ionizing radiated. See Ionizing radiated frozen egg microbial lethal effect of ionizing radiation in, 210 Frozen-stored irradiated meat versus refrigerated storage, 131 Fructose, 46 Fruit, irradiation of, 169-184. See also Produce Fruit flies, 145, 150, 151, 152–153, 156–157, 158 Fruit juice, furan and, 40 FSA. See Farm Service Agency (FSA) FSIS, 5 5-FU. See 5-Fluorouracil (5-FU) Fungi, 227 phytopathogenic, 171 resistance of, to radiation, 171 Furan, 43 apple juice and, 40 carbohydrates and, 39–40 Furyl furamide, 190 b-Galactosidase, 53 Gallate, 138–139 Gallic esters, 137 Gamma radiation, 280 Gamma ray electron beam, and X-ray technologies, advances in, for food irradiation, 11–36 basic irradiation concepts and, 12–14 electron beam facilities and, 19–28 gamma ray facilities and, 14–18, 19

300

Index

Gamma ray (continued) X-ray facilities and, 29–30, 31, 32 produce and, 170 Gamma-ray facility, 14–18, 19 commercial, 117–118, 120 operating in continuous mode, 122 GAO. See General Accounting Office (GAO) GAPs. See Good agricultural practices (GAPs) Gas chromatography, volatile hydrocarbons and, 94–95, 96 Gas evolution, macroscopic physicobiological parameters of food and, 97 Gelling qualities of eggs, 199, 204, 209 Gender, effect of, on consumer acceptance, 75 Gene expression profiling, 53 General Accounting Office (GAO), 238–239, 263 General Codex Methods, 86 Generic dose concept, 152, 153–154 Generic irradiation concept, 153 Generic irradiation treatments, 152 Generic regulations, 39 Generic treatments, phytosanitary, 152–154 Genotoxicity, 2-ACB, 52 Germination inhibition, macroscopic physico-biological parameters of food and, 98 Glenn, John, 76 Globalization of trade in food and agricultural commodities, 68 Glucose, 46, 210 Glutamine, 136 Glyceraldehydes, 136 Glycine, 136 GMPs. See Good manufacturing practices (GMPs) GNB, 98 Go/no-go indicators, product control and, 123 Good agricultural practices (GAPs), 224–225 Good manufacturing practices (GMPs) combination of, with irradiation, 190 nuts and, 224–225

Graphite as reference material, 118 GRAS food additives, 53–54 Gray discoloration in irradiated raw red meat, 134 Gray (Gy), 12–13, 107 Gray*Star Genesis Co-60 irradiator, 17, 19 Greenman v.Yuba Power Products, 265 Green tea, 249, 256–257 Ground beef, irradiated. See Irradiated ground beef “Guidelines for the Use of Irradiation as a Phytosanitary Treatment,” 159–160 Gy. See Gray (Gy) HACCP program. See Hazard Analysis Critical Control Points (HACCP) program Half-entrance depth (R50e) as range parameter, 118, 119 Half-value depth (R50) as range parameter, 118, 119 Harvesting of nuts, 222 Haugh unit, eggs and, 201 Hawaii, 6–7, 152, 153, 154, 156, 158 Hawaii Pride LLC, 153 Hazard Analysis Critical Control Points (HACCP) program, 5, 80–81, 186, 239, 268, 283–284 Headspace atmosphere in packages, 176–177 Health and Human Services, Department of, 40, 240 Health Canada, 45 Heat, ionizing radiation and, 215 Heat pasteurization of eggs, 199–200 Heat treatment of produce, 172 HeLa human cell line, genotoxicity of 2-ACBs in, 52 Heme, 55–56, 138 Hemiptera, 144 Hemolytic uremic syndrome (HUS), 5, 239 Hepatitis A, 281 green onions and, 280 manufacturing defects and, 267

Index school illness and, 239 seafood and, 185 1-Heptene, 132 Hevea brasiliensis, 48 Hexanal, 131, 230 Hexanoic acid, 230 1-Hexene, 132 High dose approach, generic dose concept and, 153–154 High hydrostatic pressure, ionizing radiation and, 215 Highly susceptible populations, legal duty for use of irradiated foods for, 269–273 his3 gene, 54 HIS3+ gene, 54 Histamine, 46, 254 Honeysuckle, Japanese, 257 Horizontal transmission of microorganisms, 199 Horticultural commodies, irradiation as phytosanitary treatment for. See Phytosanitary treatment for fresh horticultural commodities, irradiation as Hot water treatment combination of, with irradiation, 179 mangoes and, 160 HT-29 human cell line, genotoxicity of 2-ACBs in, 52 Huisken Meats, 78–79 Humidity, sensitivity of microbial cells to irradiation and, 228–229 Hurdle approach pathogen reduction and, 80 seafood salad safety and, 187 HUS. See Hemolytic uremic syndrome (HUS) Hydrocarbons, 132, 137 long chain, 216 radiolytic, 95–96 volatile, 85, 94 Hydrogen peroxide biofilms and, 172 microcidal effect and, 129 Hydrogen radicals, 231 Hydrogen sulfide, 132 Hydrolysis, enzymatic, 99

301

Hydroperoxidation, destruction of carotenoids by, 208 Hydrostatic pressure, high, ionizing radiation and, 215 Hydroxyapatite, ESR signal measurement in, 89 Hydroxyl radicals, 131, 203 Hypoxia, varietal testing and, 150 Hystidine, 209 IAEA, 29, 249 IAEA 2002, 111 IBA, 23–24, 29–30 IBA-RDI Dynamitron, 24, 25 ICGFI. See International Consultative Group on Food Irradiation (ICGFI) ICMSF. See International Commission on Microbiological Specifications for Foods (ICMSF) ICPM. See Interim Commission on Phytosanitary Measures (ICPM) ICT. See Insulating Core Transformer (ICT) IDIDAS. See International Database of Insect Disinfestation and Sterilization (IDIDAS) IgE ELISA inhibition test, 250, 251 Ignorance, negligence and, 270 Illness, foodborne. See Foodborne illnesses ILU systems, 26–27 Immune function, impaired, 269–270 Immunization, 63, 66, 81 IMPELA linac, 26 Income, effect of, on consumer acceptance, 75 Increased antioxidant capacity by irradiation, 178 Indianmeal moth, 223, 227 Inductive systems, constant-potential accelerators and, 23 Industrial linacs for radiation processing, 25–26 Information consumer acceptance and, 70 unfavorable, effect of, on consumers, 72–74

302

Index

Infrared pulsed laser beam excitation, 90–91 Insect disinfestation as goal of food irradiation, 4 nuts and, 221, 222, 223, 227 Insects, 153 artificial inoculation of, 148 large-scale confirmatory testing of, 146–147 radiotolerance of, phytosanitary treatment and, 144, 145, 146–147 sterile, 143–144, 145 Insulating Core Transformer (ICT), 23 Intensity modulated beams, 286 Interim Commission on Phytosanitary Measures (ICPM), 159 Internalization of bacteria, 172 International Atomic Energy Agency, 85, 153 International Commission on Microbiological Specifications for Foods (ICMSF), 185 International Consultative Group on Food Irradiation (ICGFI), 152 International Database of Insect Disinfestation and Sterilization (IDIDAS), 153, 154 International harmonization, phytosanitary treatment and, 159–160 International Organization for Standardization (ISO), 106 International Plant Protection Convention (IPPC), 154, 159, 160 International Standard for Phytosanitary Measures (ISPM), 159–160 Intrachromosomal recombination, 54 Inventory control procedures, 123 Ionization, irradiation and, 128 Ionization chambers, 108–109 Ionizing radiated dried egg, 208–210 functional properties of, 209–210 physicochemical properties of, 209 quality of, 208–209 Ionizing radiated egg white functional properties of, 207 physicochemical properties of, 206 quality of, 206

Ionizing radiated egg yolk functional properties of, 207–208 physicochemical properties of, 207 quality of, 207 Ionizing radiated frozen egg, 210–211 functional properties of, 211, 212–213, 214 physicochemical properties of, 210–211 Ionizing radiated liquid whole egg, 203 physicochemical properties of, 205–206 quality of, 205 Ionizing radiated shell-eggs, 200–204 functional properties of, 204 internal quality of, 201–203 physicochemical properties of, 203 Ionizing radiation application of irradiation for development of traditional fermented foods and, 257–258 biogenetic amines reduction and, 252–254 chlorophyll breakdown and, 256 color improvement of plant extracts without change of biological functions and, 256–257 of dried egg. See Ionizing radiated dried egg of eggs. See Eggs, ionizing radiation of of frozen egg. See Ionizing radiated frozen egg of liquid egg white. See Ionizing radiated egg white of liquid egg yolk. See Ionizing radiated egg yolk of liquid whole egg. See Ionizing radiated liquid whole egg microbial lethal effect of. See Microbial lethal effect of ionizing radiation potential applications of, 249–262 of produce, 170 reduction of food allergies by, 250, 251 reduction of phytic acid and increase in antioxidant activity and, 255–256

Index of refrigerated liquid egg, 204–208 volatile N-nitrosamine and residual nitrite reduction and, 251–252, 253, 254 Iotron Industries Canada Inc., 26 IP6. See Myoinositol hexaphosphate (IP6) IPPC. See International Plant Protection Convention (IPPC) Iron, phytic acid and, 255 Irradiated dry foods, rehydration of, 91 Irradiated egg products, strategies to improve quality of, 215–216 Irradiated foods. See also Food irradiation CEN method for detection of, 87, 90–91 consumer acceptance and marketing of. See Consumer acceptance and marketing of irradiated foods detection of. See Detection of irradiated foods ionizing. See ionizing irradiated entries; irradiated entries packaging of, 37–42 toxological safety of. See Toxological safety of irradiated foods Irradiated ground beef marketing of, 78–79 for National School Lunch Program, 237–248 foodborne illnesses in school and, 238–239 regulatory allowance and specifications of irradiated foods for schools and, 239–241 sensory properties of irradiated ground beef and, 241–246 Irradiated Ground Beef Education Initiative, 77 Irradiated ingredients, low-dose irradiated plants and, 98–99 Irradiated plants, low-dose, irradiated ingredients and, 98–99 Irradiated seafood, physical, chemical, and sensory changes of, 191–192

303

Irradiation basic concepts of, 12–14 combination of, with other postharvest techniques, 178–180 as effect post-processing treatment for fish products, 187–191 food. See Food irradiation; Irradiated foods generic, 152 increased antioxidant capacity by, 178 low-dose, of fresh and fresh-cut produce. See Low-dose irradiation of fresh and fresh-cut produce of nuts, 226 of nuts. See Nuts, irradiation treatment of organizations that approve or endorse, 65 as phytosanitary treatment for fresh horticultural commodities. See Phytosanitary treatment for fresh horticultural commodities, irradiation as as a Phytosanitary Treatment for Imported Fresh Fruits and Vegetables, 158 in the Production, Processing and Handling of Food, 156 quality changes in meat by. See Quality changes in meat by irradiation versus radioactivity, 69 regulatory aspects of, phytosanitary treatment and, 154–156 of seafood. See Seafood, irradiation of, with particular emphasis on Listeria monocytogenes in ready-to-eat products as tool to improve food safety, 67–68, 69 Irradiation kinetics of enteric viruses, 280 Irradiation quarantine treatments, 144, 145, 146–147 Irradiator accelerator, 118 Gray*Star Genesis Co-60, 19 MDS Nordion Centurion Co-60, 18

304

Index

Irradiator (continued) panoramic, 16–17 self-contained, 17 Irradiator dose mapping, dosimetry and, 115–117 ISO. See International Organization for Standardization (ISO) ISO/ASTM standards, 107, 111, 112, 115, 119, 283, 285 Isoleucine, 133 Isoprene, 48 ISPM. See International Standard for Phytosanitary Measures (ISPM) Japan, 153, 156 Japanese honeysuckle, 257 Jefferson Davis Associates, 72, 77–78 Joint FAO/IAEA/WHO Expert Committee, 29 Jones, Jim, 69 Journal of the American Dietetic Association, 67 Kansas State University, 70 Kay, Steve, 66 Ketoglutarate, 136 Ketones, lipid peroxidation and, 229 kg. See Kilogram (kg) kGy. See Kilogray (kGy) Kidney failure, school illness and, 239 Kilogram (kg), 12–13 Kilogray (kGy), 12–13 Kilowatt (kW), 12–13 Klystron, 25, 26–27 Klystron microwave amplifier, microwave linear accelerators and, 24 Korean fermented soybean paste, 254 Korean salted and fermented food, 257 kW. See Kilowatt (kW) K(x). See Area processing coefficient (K(x)) Lactic acid, 190–191, 193 Lactic acid–producing bacteria and yeast strains, 257 LAL/GNB See Limulus Amoebocyte Lysate/Gram Negative Bacteria (LAL/GNB)

LAL test. See Limulus Amoebocyte Lysate (LAL) test Larva stage, tolerance to irradiation and, 145–148 Laser beam excitation, infrared pulsed, 90–91 Latex allergy, 272 Lauric acid, 48 Lawsuits, 80 Legal duty for use of irradiated food, 269–273 Legal incentives in favor of food irradiation, strict liability and, 267–269 Legal perspective, food irradiation from, 263–278 challenge of highly susceptible populations and, 269–273 liability for manufacture of defective food product and, 264–267 possibility of liability arising from irradiated foods and, 273–275 possible existing legal duty to use irradiated food and, 269–273 strict liability and, legal incentives in favor of food irradiation and, 267–269 Lepidoptera, 144 Lethal effect, microbial. See Microbial lethal effect of ionizing radiation Leucine, 133 Liability arising from irradiated foods, possibility of, 273–275 legal incentives in favor of food irradiation and, 267–269 for manufacture of defective food product, 264–267 modern rule of, 265–266 in tainted food cases, origins of, 265 Licorice, 257 Light, detectable, luminescence and, 89–90 Lignin, 89 Limulus Amoebocyte Lysate/Gram Negative Bacteria (LAL/GNB), 86 Limulus Amoebocyte Lysate (LAL) test, 98 Linacs. See Linear accelerators (linacs)

Index Linac Technologies S.A., 25–26 Linear accelerators (linacs), 22 industrial, for radiation processing, 25–26 microwave, 22, 24–26 Linear shaped mtDNA, 93 Linoleic acid, 48, 50, 221, 230 Linolenic acid, 48, 221 Lipid content of fish, 192 Lipid oxidation, 131, 132, 133 Lipid peroxidation, 229–231 Lipid radiolysis, 229–231 Lipids, 46, 94–96, 97 Liposomes, 133 Liquid egg, refrigerated, ionizing radiation of, 204–208 Liquid egg white, ionizing radiation of, 206–207 Liquid egg yolk, ionizing radiation of, 207–208 Liquid whole egg (LWE), 203 ionizing radiated. See Ionizing radiated liquid whole egg ionizing radiation of, 205–206 microbial lethal effect of ionizing radiation in, 205 Listeria, 281 lawsuits and, 80 prevention of, by food irradiation, 69 reduction in, 68 Listeria monocytogenes, 4–5, 130, 188–189, 193 biofilms and, 172 D10 values for, 174–175 eggs and, 201 irradiation of seafood with particular emphasis on, in ready-to-eat products, 185–198 nuts and, 228 regrowth of, 173 seafood and, 186 Litigation, 80 Logit, insect irradiation studies and, 149 Long chain hydrocarbons in detection of prior irradiation treatment of eggs, 216 Low-dose electronic pasteurization, dosimetry and, 284–285

305

Low-dose irradiated plants, 98–99 Low-dose irradiation of fresh and freshcut produce, 169–184 irradiation to enhance microbial safety of produce and, 171–175 produce microbiology and irradiation treatment and, 170–171 safety and, 169–184 sensory characteristics of, 169–184 shelf life and, 169–184 Low-fat fish, effect of irradiation on, 187 Low redox potential of irradiated beef, 139 Low temperature, ionizing radiation and, 215 Lucigenine, 91 Luminescence, 91 free radicals and, 89–91 photo-stimulated, 86 Luminol, 91 L* values, color, 135, 137 LWE. See Liquid whole egg (LWE) Lysine, 209 Macroscopic physico-biological parameters, detection of irradiated foods and, 96–98 Maillard reaction, glucose and, 210 Male insects, tolerance of, to irradiation, 148 Malfunction doctrine, 267 Malonaldehyde, 45 Mango, 155, 160 Mango seed weevil, 151 Manufacturing defects, liability and, 266–267 Manufacturing practices, good. See Good manufacturing practices (GMPs) MAP. See Modified atmosphere packaging (MAP) Mapping dose. See Dose mapping irradiator dose, 115–117 product dose, 119–120 Marketing of irradiated foods. See Consumer acceptance and marketing of irradiated foods

306

Index

Marketing (continued) of irradiated ground beef, 78–79 liability and, 266 Market research studies, consumer acceptance and, 70 Masefield, John, 69 Mass processing rate, 13 Mass spectrometry, 95 Maximum absorbed dose (Dmax), 106, 120 Maximum pest limit, definition of, 152 Mazetti v.Armour & Company, 265 MB. See Methyl bromide (MB) MDS Nordion, 29–30 MDS Nordion Centurion Co-60 irradiator, 17, 18 MDS Nordion Co-60 pencil, 15 MDS Nordion Co-60 source rack, 16 MDS Nordion Pallet, 16–17 Mealybugs, 153 Mean energy of electron beam, accelerator facility and, 118 Measured dose value, traceable, dosimetry and, 111 Meat color changes in, by irradiation, 134–137 mechanically recovered, 99 off-odor in, 127–128, 137–139 quality changes in, by irradiation. See Quality changes in meat by irradiation Meat thermometers, use of, 67 Mechanically recovered meat (MRM), 99 Mechanisms and prevention of quality changes in meat by irradiation. See Quality changes in meat by irradiation Mediterranean fruit fly, 150, 152–153, 156 Meeting of the Parties to the Montreal Protocol, 157 Melon fruit fly, 152–153, 156 Mercaptomethane, 132 Mesophilic aerobes, 210 Metal chelating agents, 137 Methane, 128 Methane thiol, 231

Methionine, 133, 209 Methyl bromide (MB) effect of, on ozone layer, 6, 157, 225 nuts and, 222, 225 2-Methyl butanal, 132, 133 3-Methyl butanal, 132, 133 2-Methylcyclobutanone, 48 Methyl esters of parahydroxybenzoic acid, 190 Methyl mercaptan, 132 Methyl thioacetate, 132 Mevex Corporation, 25–26 Microbial contamination of nuts, 222–224 Microbial ecology, phytoplane, 171 Microbial lethal effect of ionizing radiation in dried egg, 208 in egg white, 206 in frozen egg, 210 in liquid whole egg, 205 on shell-eggs, 200–201 Microbial load, reduction of, 170–171 Microbial pathogens, 156 Microbial radiation sensitivity, 215 Microbial reduction as goal of food irradiation, 4–6, 170–171 Microbial risk assessment, 283–284 Microcidal effect, food irradiation and, 129–130 Micrococcus, 223 Micro-electrophoresis, single gel, 86 Microflora, competing, 191–192 Microscopic fluorescence, 98 Microtox Assay, 53–54 Microwave, electromagnetic, 86–88 Microwave linear accelerators, 22, 24–26 Milk, certified raw, 63 Minimum absorbed dose (Dmin), 106, 120, 121 Minnesota Beef Council, 76 Minnesota Beef Research & Promotion Council, 78 Minnesota Department of Health, 76–77, 78 Minnesota Model of consumer acceptance, 76–78 Minnesota State Fair, 77

Index Mites, 153 Mitochondrial DNA (mtDNA), 93 Model Food, FDA, 271 Modified atmosphere packaging (MAP), 178, 193, 285 Moisture, sensitivity of microbial cells to irradiation and, 228–229 Mold, 221, 222–224, 227–228 Monounsaturated fatty acids, 133 Monte Carlo calculations, 13 Monte Carlo coefficients, 21 Monte Carlo simulation, 30 Monte Carlo stimulation, 29 Montreal Protocol, 6, 157 Moths, 153, 154, 158, 227 MRM. See Mechanically recovered meat (MRM) mtDNA. See Mitochondrial DNA (mtDNA) m-tyrosine, 92 Multiple barrier approach, pathogen reduction and, 80 Mutagenesis assays, forward, 53 Mutagenicity cooked meats and, 43 irradiation and, 40 Mutations, 43 Myoglobin, 139 ferric, 138 Myoinositol hexaphosphate (IP6), 255 Myristic acid, 48, 97 NAFTA. See North American Free Trade Agreement (NAFTA) NAPPO. See North American Plant Protection Organization (NAPPO) National Cattlemen’s Beef Association, 70, 75–76 National Food Processors Association (NFPA), 226 National School Lunch Program, irradiated ground beef for. See Irradiated ground beef for National School Lunch Program Navel orangeworm, 223, 227 NDMA. See Nitrosodimethylamine (NDMA); N-Nitrosodimethylamine (NDMA)

307

Negative information, consumer acceptance and, 73–74 Negligence failing to avoid risks and, 270–271 manufacturing defects and, 267 proof of, liability for manufacture of defective food product and, 264 Nematodes, tolerance of, to irradiation, 144, 145 New technology, resistance to, by consumers, 64, 65 New Zealand, 7, 153 Nfo DNA gene, 53 NFPA. See National Food Processors Association (NFPA) Nissin High Voltage, 23 NIST, 108 Nitrite sausage and, 253 smoked fish and, 194 Nitrite reduction, residual, 251–252, 253, 254 N-Nitrosamine reduction, 251–252, 253, 254 Nitrosamines, 43, 46 N-Nitrosamines, 253 Nitrosodimethylamine (NDMA), 46, 252 N-Nitrosodimethylamine (NDMA), 254 Nitrosopyrrolidine (NPYR), 46, 252 N-Nitrosopyrrolidine (NPYR), 254 Nondiapausing strains of insects, tolerance of, to irradiation, 148 Nonenal, 132 2-Nonenal, 53–54 1-Nonene, 132 Nonfood phytosanitary treatments, 161–163 Nonfruit fly pests, 153 Nonmortality treatment of quarantine pests, 157 Nonoxidative radiolytic reactions, 231 Nonsulfur amino acid homopolymers, 134 Nonuniform products, dose mapping of, 119 Noroviruses, 280–281 Norovirus surrogates, 281

308

Index

North American Free Trade Agreement (NAFTA), 159 North American Plant Protection Organization (NAPPO), 159, 160 Norwalk-like viruses, 239 Norwalk virus, 185 NPL, 108 NPL Report CIRM 29, 111 NPYR. See Nitrosopyrrolidine (NPYR); N-Nitrosopyrroline (NPYR) Nucleic acids effect of radiation on, 282 radiolytic products from, detection of irradiated foods and, 93–94 Nutrition, tumor production and, 55–56 Nuts irradiation treatment of, 221–236 advantages of, 231–232 aflatoxins and, 227–228 chemical and sensory, 229–231 contamination with pathogens and, 224–226 farming and harvesting of, 222 insect disinfestation and, 222, 223, 227 lipid peroxidation and, 229–231 microbial contamination and, 222–224 molds and, 227–228 pathogen inactivation and, 228–229 protein radiolysis and, 229–231 research in, 232 pathogenic microbial control and, 225–226 Nymph stage, tolerance to irradiation and, 145–148 1-Octene, 132 Off-odor in eggs, 203 in meat, 127–128, 137–139 O-glycosides in eggs, 202 Oil components, dietary, colon cancer and, 55 OIRSA. See Organismo Internacional Regional de Sanidad Agropecuaria (OIRSA) Oleic acid, 48, 50, 95, 96, 230

Omaha Steaks, 79 Oncogenes, 43 Open circular mtDNA, 93 Operating cost, low-dose electronic pasteurization and dosimetry and, 284–285 Operational qualification, dosimetry and, 106, 115–118 Optimum thickness (Ropt), 118, 119 Orangeworm, navel, 223 Ordinary care, definition of, and negligence, 270 Organismo Internacional Regional de Sanidad Agropecuaria (OIRSA), 159 Organoleptic changes caused by radiation, 191 Oriental fruit fly, 151, 152–153 ORP. See Oxidation-reduction potential (ORP) o-tyrosine, 92 Ovalbumin, 203, 206, 216 Ovomucin, 203 Ovomucin protein moiety in eggs, 202 Ovomucoid, 206, 216 Ovotransferrin, 206 Oxidation, lipid, irradiation and, 131 Oxidation-reduction potential (ORP), 136, 138 Oxidative/radiolytic cleavage of phenylalanine, 45 Oxidized beef fat, colon cancer and, 55 Oxidized heme, colon cancer and, 55–56 Oxygen lipid oxidation and, 131 nuts and, 225 radiation tolerance and, 215 as scavenger of aqueous electrons, 137–138 varietal testing and, 150 oxyMb-like pigment. See Oxymyoglobin (oxyMb)-like pigment Oxymyoglobin (oxyMb)-like pigment, 136 Ozone biofilms and, 172 effect of methyl bromide on, 6, 157, 225

Index Packaging, 7, 132, 137 botulism and, 193 complex-shaped, 285–286 in control of off-odor production and color changes in meat, 138–139 double, 138–139 effect of, on color and off-odor, 134–135, 139 modified atmosphere, 178, 193, 285 regulation of, 37–42 research and, 285 respiration rate and headspace atmosphere in, 176–177 vacuum. See Vacuum packaging Palletron rotational X-ray irradiation system, 29–30, 31, 32 Pallets of food, irradiation of, 8 Palmitic acid, 47, 48, 50, 95, 96, 97 Palmitoleic acid, 48 Panoramic irradiator, 16–17 Paracelsus, 56 Parahydroxybenzoic acid, methyl and propyl esters of, 190 Parallel-coupled systems, accelerators and, 23, 24 Parallelism, insect irradiation studies and, 149 Parallel systems, constant-potential accelerators and, 23 Pasteur, Louis, 63, 78 Pasteurization, 81 cold, 64, 274 critics of, 63–64 electronic. See Electronic pasteurization; Food irradiation; Irradiated foods risks versus benefits of, 66 Pathogenic microbial control, 225–226 Pathogens bacteria, fungi, and viruses and, 171 bacterial, research and, 281–282 contamination with, 224–226 foodborne, D-values of, 130 inactivation of, 228–229 protozoan, 281 target, 280–282 Peace twig borer, 223

309

Peptone, shielding effects of, 282 Peroxidation in eggs, 208, 209 Peroxide value (POV), 256 Persimmon leaf, 257 Pest control, 223, 225 Pests, 143, 145 Petitions, FDA, 38 Phenol acids, 256–257 Phenolic compounds, irradiation and, 178 Phenylalanine, 45, 92 b-Phenylethylamine, 254 pH of eggs, 203, 207, 209 Phosphine, 222, 225 Phospholipids, 136 Phosphorous, phytic acid and, 255 Photon sources of ionizing radiation, 170 Photo-stimulated luminescence (P.S.L.), 86 Physicobiological parameters, detection of irradiated foods and, 96–98 Physicochemical properties of ionizing radiated dried egg, 209 of ionizing radiated egg white, 206 of ionizing radiated egg yolk, 207 of ionizing radiated frozen egg, 210–211 of ionizing radiated liquid whole egg, 205–206 of ionizing radiated shell-eggs, 203 of irradiated seafood, 191–192 irradiation-induced, 203 Physics, radiation, 282–285 Phytic acid reduction, irradiation and, 255–256 Phytopathogenic fungi, 171 Phytoplane microbial ecology, 171 Phytosanitary treatment for fresh horticultural commodities, irradiation as, 143–168 developing irradiation quarantine treatments and, 144, 145, 146–147 generic treatments and, 152–154 methodology of, 145–149 Probit 9 efficacy and alternatives and, 150–152

310

Index

Phytosanitary treatment (continued) regional and international harmonization and, 159–160 regulatory aspects of irradiation and, 154–156 trade and, 160–163 USDA regulations and, 156–158 varietal testing and, 150 Plaintiff rule, eggshell, liability and, 271–272 Planktonic bacteria, 173 Plant extracts, improvement in color of, 256–257 Plants low-dose irradiated, irradiated ingredients and, 98–99 variety of, effect of irradiation on, 174–175 Plum curculio, 158 PMMA. See Polymethylmethacrylate (PMMA) PMMA dosimeters, 109, 112 Point mutations, 43 Point of use (POU) filtration devices, 283 Poliovirus type 1, 282 Polyethylene, electron beam penetration in, 20 Polymethylmethacrylate (PMMA), 107 Polyphenols, 137, 256 Polyploidy, 40 Polystyrene, 118 Polyunsaturated fatty acids (PUFA), 133 Pork patties, 257 Positive information, consumer acceptance and, 73–74 Postharvest techniques, combination of irradiation with, 178–180 Post-irradiation dosimetry, accidental, 89 Post-irradiation recovery and regrowth of pathogens, 173 Post-processing contamination, 186 Potassium lactate, 191 Potassium sorbate, 190, 193 Potatoes, electric impedance of, 97 POU filtration devices. See Point of use (POU) filtration devices

POV. See Peroxide value (POV) Practical range (Rp), 118, 119 Precision, dosimetry and, 111 Primary-standard dosimeters, 107–109 Probit 9 nuts and, 225 phytosanitary treatment and, 150–152 Probit analysis, insect irradiation studies and, 149 Process control, routine, dosimetry and, 114, 122–124 Processing, food, dosimetry for. See Dosimetry Process parameters, dosimetry and, 122 Process qualification, dosimetry and, 106, 118–121 Process validation, dosimetry and, 114–115 Produce fresh and fresh-cut, low-dose irradiation of. See Low-dose irradiation of fresh and fresh-cut produce irradiation to enhance microbial safety of, 171–175 microbiology and irradiation treatment of, 170–171 sanitization of, 172 treatment parameters for irradiation of, 173–174 Produce-associated foodborne illness, 169 Product, definition of, liability and, 266 Product certification, dosimetry and, 123–124 Product control, dosimetry and, 123 Product dose mapping, dosimetry and, 119–120 Product overlap, gamma-ray facilities and, 120 Product packaging. See Packaging Product release, dosimetry and, 123–124 Profiling, gene expression, 53 Prooxidants, lipid peroxidation and, 230

Index Propylene oxide, 225, 228, 230 Propyl esters of parahydroxybenzoic acid, 190 Protein radiolysis, 229–231 Proteins, 203 in detection of prior irradiation treatment of eggs, 216 radiolytic products from, 92 Protozoan pathogens, 281 Pseudomonas, 223 PSL See Photo-stimulated luminescence (PSL) p-tyrosine, 92 Public Citizen, 240, 273 Public health, potential annual benefits of, food irradiation and, 69 PUFA. See Polyunsaturated fatty acids (PUFA) Pulsed laser beam excitation, infrared, 90–91 Punitive damages as incentive, negligence and, 272–273 Pupa stage, tolerance to irradiation and, 145–148 Pure aqueous carbohydrate solutions, radiolysis of, 92–93 Pure triacylglycerides, 50 Putrescine, 46, 253, 254 Pyralid pests, 154 Pyruvate, 136 Quality assurance, dosimetry measurements and, 106 Quality changes in meat by irradiation, 131–139 color changes and, 134–139 future research on, 139 lipid oxidation and, 131 mechanisms and prevention of, 127–142, 128–129 microcidal effect and, 129–130 off-odor production and, 131–134, 137–139 in produce by irradiation, 175–180 Quarantine pests, 143, 145 Quarantine treatment for fresh horticultural commodities, irradiation as, 143–168

311

irradiation, development of, phytosanitary treatment and, 144, 145, 146–147 Quenching molecules, nucleic acids and, 282 R50. See Half-value depth (R50) rad, 12 Radiation food additives and, 38 ionizing. See Ionizing radiation ultraviolet, 11 Radiation dosimetry, 90 Radiation energy, 128 Radiation-induced formation of 2-ACBs from precursor fatty acids, 48, 49–50 Radiation physics and chemistry, 282–285 Radiation power, emitted, absorbed dose versus, 12–13 Radiation processing, industrial linacs for, 25–26 Radiation-sensitive indicators, product control and, 123 Radiation sensitivity, microbial, 215 Radiation tolerance, varietal testing and, 150 Radicals, 88 free. See Free radicals hydrogen, 231 hydroxyl, 131, 203 Radical scavengers, 281-282. See also Free radicals Radioactivity versus irradiation, 69 Radiochromic dosimeters, 109 Radiochromic film, 107, 112, 113 Radio-frequency accelerators, 26–28 Radio-frequency resonant cavity systems, 22 Radiolysis amino acid, 133 lipid, 229–231 protein, 229–231 of pure aqueous carbohydrate solutions, 92–93 of water, microcidal effect and, 129 Radiolytic cleavage of phenylalanine, 45

312

Index

Radiolytic hydrocarbons, 95 Radiolytic products, 73, 74 from carbohydrates, 92–93 from lipids, 94–96 from nucleic acids, 93–94 primary, 85 from proteins, 92 secondary, 85 stable, 91–96 Radiolytic reactions, nonoxidative, 231 Radiotolerance, insect, phytosanitary treatment and, 144, 145, 146–147 Range, practical, as range parameter, 118 Rats,Wistar, 54 Raw meat, color changes in, by irradiation, 134–135 Raw milk, certified, 63 RDI, 29 R50e. See Half-entrance depth (R50e) Ready-to-eat (RTE) products, 185, 226 additives and, 139 irradiation of seafood with particular emphasis on Listeria monocytogenes in, 185–198 RecA gene, 53 RecA regulator, 130 Recombination, free radicals and, 128–129 Records, product release and certification and, 123–124 Redness in irradiated light meats, 134 Reduction of food allergies, 250, 251 Reference monitoring location, dosimetry and, 121 Reference-standard dosimeters, 108–109 Refrigerated liquid egg, 204–208 Refrigerated storage versus frozenstored irradiated meat, 131 Regional harmonization, phytosanitary treatment and, 159–160 Regrowth of pathogens, post-irradiation, 173 Regulations generic, 39 of irradiated foods and packaging, 37–42

irradiated foods for schools and, 239–241 irradiation as phytosanitary treatment for fresh horticultural commodities and, 143–168 Rehydration of irradiated dry foods, 91 Remedial measures, subsequent, negligence and, 268–269 Reovirus, 281 Research dosimetry for. See Dosimetry in ionizing radiation of eggs, 216 irradiation as phytosanitary treatment for fresh horticultural commodities and, 143–168 irradiation of nuts and, 232 market, consumer acceptance and, 70 in quality changes in meat, 139 and technical challenges in electronic food pasteurization, 279–287 complex-shaped packages and, 285–286 product packaging and, 285 radiation physics and chemistry and, 282–285 target pathogens and, 280–282 Residual nitrite reduction, 251–252, 253, 254 Respiration rate in packages, 176–177 Rhodotron six-pass IBA, 26 ten-pass IBA, 28 Richard B. Russell National School Lunch Act, 240 Risks versus benefits, 64, 66 failing to avoid, negligence and, 270–271 microbial, assessment of, 283–284 Root, green tea and, 257 Ropt. See Optimum thickness (Ropt) Rotavirus, 281 Routine dosimetry, 108–109, 122 Routine process control, dosimetry and, 106, 114, 122–124

Index Routine product dosimetry, dosimetry and, 122–123 Rp. See Practical range (Rp) Safety food. See Food safety low dose irradiation of fresh and fresh-cut produce and, 169–184 and Nutritional Adequacy of Irradiated Foods, The, 44 toxological, of irradiated foods. See Toxicological safety of irradiated foods Safety track, food, 4–6 Salmonella, 4, 54, 127, 130, 229, 281 biofilms and, 172–173 D10 values for, 174–175 in eggs, 204, 205, 206 eggs and, 199, 200, 201, 208 5-fluorouracil and, 53 foodborne illnesses in children and, 238 frozen whole egg and, 210 ground beef and, 241 irradiated poultry and, 72 lawsuits and, 80 manufacturing defects and, 267 negligence and, 270 nuts and, 224, 225–226, 228, 231, 232 outbreak of, in Chicago restaurant, 264, 268 prevention of, by food irradiation, 69 reduction in, 68 school illness and, 239 seafood and, 185 thermoradiation and, 215 Salmonella Mutagenicity Test (SMT), 52–53 Salted foods gamma irradiation and, 258 Korean, 257 Salting, combination of, with irradiation, 188–190 Sanitization combination of, with irradiation, 178–179 of produce, 172 Satin, Morton, 68, 79, 81

313

Saturated fatty acids, 133 S-band systems, 24–26 Scan width, accelerator facility and, 118 Scavengers, 126. See also Free radicals Schools breakfast program in, 237 foodborne illnesses in, 238–239 national lunch program for, 237–248 Schwan’s, Inc., 79 Seafood. See also Fish irradiation of, with particular emphasis on Listeria monocytogenes in ready-to-eat products, 185–198 chemical changes of irradiated seafood and, 191–192 competing microflora and, 192–193 irradiation as effective postprocessing treatment for fish products and, 187–191 Listeria monocytogenes as significant contaminant of seafood and, 185–186 physical, chemical, and sensory changes of, 191–192 risk for botulism and, 193–194 sensory changes of irradiated seafood and, 191–192 stress adaptation of organism and, 187 smoked, 186 stress adaptation of, 187 Seafood salad, 186, 187, 191, 192 Selective supercritical carbon dioxide extraction, 96 Self-contained irradiator, 17 Sensitizers, free radicals and, 129 Sensory properties of irradiated ground beef, 241–246 of irradiated seafood, 191–192 low-dose irradiation of fresh and fresh-cut produce and, 169–184 radiation-degradation of, 216 Series systems, constant-potential accelerators and, 23 Sesamol, 138–139

314

Index

Shelf-life extension of, as goal of food irradiation, 4 low dose irradiation of fresh and fresh-cut produce and, 169–184 Shell-eggs, 199, 200 ionizing radiated. See Ionizing radiated shell-eggs microbial lethal effect of ionizing radiation on, 200–201 Shells damaged, nuts and, 223 dating, ESR signal measurement in, 89 Shigella nuts and, 228 school illness and, 239 seafood and, 185 Shuffle-dwell system, 122 Shuttle Discovery, 76 Silver chromatography, 99 Sinclair, Upton, 269 Single gel micro-electrophoresis, 86 6-log reduction of target organism, 283–284 Six-pass IBA Rhodotron, 26 Slaughterhouses, Upton Sinclair and, 269 Smoked fish, 186, 194 Smoking, cold, 186 SMT. See Salmonella Mutagenicity Test (SMT) Sodium ascorbate, 136 Sodium benzoate, 190, 193 Sodium diacetate, 191 Sodium lactate, 193 Sodium polytungstate, 99 Sodium salts of methyl and propyl esters of parahydroxybenzoic acid, 190 Soft scales, 153 Sogginess, irradiation and, 176 SOS response, DNA repair and, 130 Source overlap, gamma-ray facilities and, 120 Southern fire ant, 223 Soxhlet extraction, 96 Soybean paste, Korean fermented, 254 Spectrometers, 107

Spectrometry, mass, 95 Spectrophotometers, 107 Spectroscopy electron spin resonance, 85, 86 ESR, free radicals and, 86–89 Spermidine, 46, 253, 254 Spermine, 46, 253, 254 Spices, 92, 156 Spider mites, 158 Spoilage bacteria, D-values of, 130 Spore-forming organisms nuts and, 228 resistance of, to irradiation, 193 Stable radiolytic products, detection of irradiated foods and, 91–96 Standardized protocols, radiation physics and chemistry and, 282–283 Standards ISO/ASTM, 111, 112, 115, 119, 283, 285 on Nuclear Technology and Applications, 283 USDA, 201 Staphyloccus aureus, 188–189 Staphylococcus, 223, 241 Staphylococcus aureus, 130 nuts and, 228 school illness and, 239 seafood and, 188 Starvation of exponential phase cells, 191 State Department of Agriculture, 237 of Education, 237 Steam application, 179 Stearic acid, 48, 50, 95, 96, 97 Sterile insects, 143–144, 145 Steris IsoMedix Services, 69 Storage, off-odor production in meat and, 131–132 Stossel, John, 74 Strecker degradation, 133 Streptococcus, 223, 224 Stress adaptation, 187 Stress response system, 191 Strict liability. See Liability Subsequent remedial measures, negligence and, 268–269

Index Sucrose, 46 Sugars, crystalline, 89 Sulfur amino acids, 133 Sulfur compounds, 132, 133 Sulfur-containing amino acids, 231 Sulfur-containing volatiles, 134 Sulfur dioxide, 132 Supercoiled mtDNA, 93 SureBeam, 4, 6 Surimi, 186, 188, 191, 192 Susceptible populations legal duty for use of irradiated foods for, 269–273 liability and, 271–272 Sweet potato weevil, 154, 158 Syracuse University, 80 TAMU. See Texas A & M University (TAMU) Target dose, dosimetry and, 121 Target pathogens, research and, 280–282 Tauxe, Robert, 68 2-tDCB, 54 2-tDeCB, 54, 55 Tea, green, 249, 256–257 Technical challenges and research directions in electronic food pasteurization. See Research and technical challenges in electronic food pasteurization Technical Consultation of Regional Plant Protection Organizations, 159 Temperature botulism and, 193 low, ionizing radiation and, 215 Temperature rise, dose versus, 13–14 Ten-pass IBA Rhodotron, 28 Tephritid fruit flies, 145, 151, 152, 153, 158 2-Tetradecylcyclobutanone, 95 Texas A & M University (TAMU), 71 “The Application of Irradiation to Phytosanitary Problems,” 158, 159 Thermoluminescence, 85, 91, 99 Thermoluminescence reader, 90 Thermoluminescent dosimetry, 284–285

315

Thermoradiation, 215 The Safety and Nutritional Adequacy of Irradiated Foods, 44 Thickness, optimum, 118 Thin film dosimeters, 116 Thin-skulled plaintiff rule, liability and, 271–272 Third Restatement of the Law,Torts: Products Liabillity, 79–80 Thrips, 153 Throughput, and dosimetry and, 284–285 Thymidine, 93 Thymine glycol, fluorescence analysis of, 93 Thysanoptera, 144 Titan Scan, 26 Tocopherol, 137, 138–139 microcidal effect and, 129 phytic acid and, 255 a-Tocopherol, 230 Toluene, 45 Tongue, canned, 265 Total aerobic count (TAC), 179 Toxicological safety of irradiated foods, 43–62 Toxin, botulin, 73 Toxological safety of irradiated foods amines and, 45–46 benzene and, 45–46 diet and tumor promotion and, 55–56 food irradiation and, 44–45 formaldehyde and, 45–46 formation and levels of 2-ACBs in foods and, 46–51 2-ACBs and, 52–55 Toxoplama gondii, 281 Toxoplasma, 69 Traceable measured dose value, dosimetry and, 111 Trade globalization of, in food and agricultural commodities, 68 phytosanitary treatment and, 160–163 Trans-fats, effect of irradiation on, 40 Transfer-standard dosimeters, 108–109

316

Index

Transovarian transmission of microorganisms, 199 Traynor, Roger, 265 Treatment parameters for irradiation of produce, 173–174 Triacylglycerides, pure, 50 Trichinella, 72 Triglycerides, 46, 47–48, 96, 133 Trimethyl sulfide, 132 Triode tubes, 26–27 Tryptamine, 46, 254 Tumor promoters, 43 Tumor promotion diet and, 55–56 2-ACBs and, 54–55 Tumor suppressor genes, 43 Turf to tort, 80 20/20 news program, 74 Tyramine, 254 Tyrosine, 209 U-235, 14 Ultraviolet (UV) radiation, 11 UmuDC gene, 53 Unfavorable information, effect of, on consumers, 72–74 Unique radiolytic product (URP), 48, 92 Unity rule, 13, 21 University of California, 70, 224 of Georgia, 71, 72 of Minnesota, 76–77 Upper-dose limit of ionizing radiation, 105 Uracil-phosphoribosyltransferase gene, 53 URP. See Unique radiolytic product (URP) U.S.Army Medical Department, 127 U.S. Centers for Disease Control and Prevention. See Centers for Disease Control and Prevention (CDC) U.S. Department of Agriculture (USDA), 5, 66–67, 74, 156–157, 240, 246, 268, 283 Agricultural Marketing Service of, 237

Economic Research Service of, 268 Food and Nutrition Service (FNS) of, 237 Food Safety and Inspection Service of, 66–67 regulations of, phytosanitary treatment and, 156–158 standards of, 201 of Health and Human Services, 40, 240 U.S. Environmental Protection Agency, 155, 283 U.S. Food and Drug Administration (FDA), 14, 29, 37, 38, 44, 127, 154, 156, 227, 283 U.S. General Accounting Office (GAO), 238–239, 263 USDA. See U.S. Department of Agriculture (USDA) USDA-APHIS, 6, 152–153, 153, 157 Use of Approved Food Safety Technology, 239–240 Utah State University, 67 UV radiation, 11 Vacuum packaging, 132, 137 effect of, on color and off-odor, 134–135, 139 seafood and, 187–188 Variable energy attenuators, 286 Varietal testing, phytosanitary treatment and, 150 Vegetables, irradiation of, 169-184. See also Produce Verification process, 120–121 Vertical transmission of microorganisms, 199 Vibrio, 4, 281–282 Vibrio fisheri, 53–54 Vibrio parahaemolyticus, 185 Vibrio vulnificus, 281–282 Viruses enteric. See Enteric viruses Norwalk-like, 239 resistance of, to radiation, 171 Vitamin C incidence of cancer and, 178 sensitivity of, to irradiation, 177

Index Vitamin E incidence of cancer and, 178 lipid peroxidation and, 230 VNAs. See Volatile N-nitrosamines (VNAs) Voids, products with, dose mapping of, 119 Volatile aldehydes, 137 Volatile food extracts, chromatograms of, 92 Volatile hydrocarbons, 85, 94 Volatile N-nitrosamines (VNAs), 251–252, 253, 254 Volatiles, 133 amino acid side chains and, 134, 139 detection of irradiated foods and, 92 eggs and, 201 sulfur-containing, 231 Warehouses, cold storage, 8 Warm water treatment, combination of, with irradiation, 179 Water dose to, 107 electron beam penetration in, 20 radiation tolerance and, 215 as reference material, 118 sensitivity of microbial cells to irradiation and, 228–229 Water wash hot. See Hot water treatment pathogen regrowth and, 173 Webbing, 222, 227 Weevil, sweet potato, 154, 158 Wegmans, 79 Whitman School of Management at Syracuse University, 80 WHO. See World Health Organization (WHO)

317

Whole chicken, dose mapping of, 119 Whole egg, liquid. See Liquid whole egg (LWE) Whole egg yolk, 203 Wistar rats, 54 Wood products, phytosanitary treatments for, 161–163 Working dosimeters, 108–109 World Health Organization (WHO), 44, 127, 240, 249 World Trade Organization, 159 WTO-SPS Agreement, 159 Xanthomonas, 223 X-ray facilities, 29–30, 31, 32 X-rays, 29–30, 170 X-ray technologies. See Gamma ray, electron beam, and X-ray technologies, advances in, for food irradiation Yeast lactic acid–producing, 257 nuts and, 222–224 Yeast DEL Assay, 54 Yersinia enterocolitica, 193, 228 Yolk gelling, freezing and, 210 Zero-risk society, 64 Zero-tolerance policy Escherichia coli and, 5 for Listeria monocytogenes in readyto-eat foods, 185 Zinc, phytic acid and, 255 Zircaloy tubes, Co-60 pencils and, 15 Zollers, Frances, 80