IMPROVING FOOD SAFETY
THROUGH A ONE HEALTH APPROACH




WORKSHOP SUMMARY







Eileen R. Choffnes, David A. Relman, LeighAnne Olsen, Rebekah Hutton,
and Alison Mack, Rapporteurs

Forum on Microbial Threats

Board on Global Health


INSTITUTE OF MEDICINE
OF NATIONAL ACADEMIES





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IMPROVING FOOD SAFETY THROUGH A ONE HEALTH APPROACH Workshop Summary Eileen R. Choffnes, David A. Relman, LeighAnne Olsen, Rebekah Hutton, and Alison Mack, Rapporteurs Forum on Microbial Threats Board on Global Health

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THE NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001 NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. Financial support for this project was provided by the American Society for Microbiology; Burroughs Wellcome Fund; GlaxoSmithKline; Infectious Diseases Society of America; Merck Company Foundation; sanofi pasteur; U.S. Agency for International Development; U.S. Department of Defense, Department of the Army: Defense Threat Reduction Agency, Global Emerging Infections Surveillance and Response System, and the Medical Research and Materiel Command; U.S. Department of Health and Human Services: Centers for Dis- ease Control and Prevention, Fogarty International Center, Food and Drug Administration, National Institute of Allergy and Infectious Diseases, and National Institutes of Health; U.S. Department of Homeland Security; and U.S. Department of Veterans Affairs. The views presented in this publication do not necessarily reflect the views of the organizations or agencies that provided support for this project. International Standard Book Number-13: 978-0-309-25933-0 International Standard Book Number-10: 0-309-25933-9 Additional copies of this report are available from the National Academies Press, 500 Fifth Street, NW, Keck 360, Washington, DC 20001; (800) 624-6242 or (202) 334-3313; http://www.nap.edu. For more information about the Institute of Medicine, visit the IOM home page at: www. iom.edu. Copyright 2012 by the National Academy of Sciences. All rights reserved. Printed in the United States of America Cover images: (Front): Courtesy of Rebekah Hutton; (Back): Adapted from Hufnagel, L., D. Brockmann, and T. Geisel. 2004. Forecast and control of epidemics in a globalized world. Proceedings of the National Academy of Sciences 101(42):15124-15129. The serpent has been a symbol of long life, healing, and knowledge among almost all cultures and religions since the beginning of recorded history. The serpent adopted as a logotype by the Institute of Medicine is a relief carving from ancient Greece, now held by the Staatliche Museen in Berlin. Suggested citation: IOM (Institute of Medicine). 2012. Improving food safety through a One Health approach. Washington, DC: The National Academies Press.

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“Knowing is not enough; we must apply. Willing is not enough; we must do.” — Goethe Advising the Nation. Improving Health.

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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal government on scientific and technical matters. Dr. Ralph J. Cicerone is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Charles M. Vest is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examina- tion of policy matters pertaining to the health of the public. The Institute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the Na- tional Academy of Engineering in providing services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph J. Cicerone and Dr. Charles M. Vest are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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FORUM ON MICROBIAL THREATS1 DAVID A. RELMAN (Chair), Stanford University and Veterans Affairs Palo Alto Health Care System, Palo Alto, California JAMES M. HUGHES (Vice-Chair), Global Infectious Diseases Program, Emory University, Atlanta, Georgia LONNIE J. KING (Vice-Chair), The Ohio State University, Columbus KEVIN ANDERSON, Biological and Chemical Defense Division, Science and Technology Directorate, Department of Homeland Security, Washington, DC RUTH L. BERKELMAN,2 Center for Public Health Preparedness and Research, Rollins School of Public Health, Emory University, Atlanta, Georgia DAVID BLAZES,3 Division of Global Emerging Infectious Surveillance, Armed Forces Health Surveillance Center, Silver Spring, Maryland ENRIQUETA C. BOND, Burroughs Wellcome Fund (Emeritus), Marshall, Virginia ROGER G. BREEZE, Lawrence Livermore National Laboratory, Livermore, California PAULA R. BRYANT, Defense Threat Reduction Agency, Medical S&T Division, Fort Belvoir, Virginia JOHN E. BURRIS, Burroughs Wellcome Fund, Research Triangle Park, North Carolina ARTURO CASADEVALL, Albert Einstein College of Medicine, Bronx, New York PETER DASZAK, EcoHealth Alliance, New York, New York JEFFREY S. DUCHIN, Public Health–Seattle and King County, Washington JONATHAN EISEN, Genome Center, University of California, Davis, California RALPH L. ERICKSON, Walter Reed Army Institute of Research, Silver Spring, Maryland MARK B. FEINBERG, Merck Vaccine Division, Merck & Co., Inc., West Point, Pennsylvania JACQUELINE FLETCHER, Oklahoma State University, Stillwater, Oklahoma CLAIRE FRASER,4 Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland JESSE L. GOODMAN, Food and Drug Administration, Rockville, Maryland 1 Institute of Medicine Forums and Roundtables do not issue, review, or approve individual docu- ments. The responsibility for the published workshop summary rests with the workshop rapporteurs and the institution. 2 Forum member until December 31, 2011. 3 Forum member until March 31, 2012. 4 Forum member since June 1, 2012. v

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EDUARDO GOTUZZO, Instituto de Medicina Tropical–Alexander von Humbolt, Universidad Peruana Cayetano Heredia, Lima, Peru CAROLE A. HEILMAN, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland DAVID L. HEYMANN, Health Protection Agency, London, United Kingdom ZHI HONG, GlaxoSmithKline, Research Triangle Park, North Carolina PHILIP HOSBACH, sanofi pasteur, Swiftwater, Pennsylvania STEPHEN ALBERT JOHNSTON, Arizona BioDesign Institute, Arizona State University, Tempe, Arizona KENT KESTER,5 Uniformed Services University of the Health Sciences, Bethesda, Maryland GERALD T. KEUSCH, Boston University School of Medicine and Boston University School of Public Health, Boston, Massachusetts RIMA F. KHABBAZ, Centers for Disease Control and Prevention, Atlanta, Georgia STANLEY M. LEMON, School of Medicine, University of North Carolina, Chapel Hill, North Carolina EDWARD McSWEEGAN, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland MARK A. MILLER, Fogarty International Center, Bethesda, Maryland JULIE PAVLIN,6 Armed Forces Health Surveillance Center, Silver Spring, Maryland GEORGE POSTE, Complex Adaptive Systems Initiative, Arizona State University, Tempe, Arizona DAVID RIZZO, Department of Plant Pathology, University of California, Davis, California GARY A. ROSELLE, Veterans Health Administration, Department of Veterans Affairs, Cincinnati, Ohio ALAN S. RUDOLPH, Defense Threat Reduction Agency, Fort Belvoir, Virginia KEVIN RUSSELL, Armed Forces Health Surveillance Center, Silver Spring, Maryland JANET SHOEMAKER, American Society for Microbiology, Washington, DC P. FREDERICK SPARLING, University of North Carolina, Chapel Hill, North Carolina TERENCE TAYLOR,7 International Council for the Life Sciences, Arlington, Virginia MURRAY TROSTLE, U.S. Agency for International Development, Washington, DC MARY E. WILSON, Harvard School of Public Health, Harvard University, Boston, Massachusetts 5 Forum member since June 1, 2012. 6 Forum member since April 1, 2012. 7 Forum member until December 31, 2011. vi

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Staff EILEEN CHOFFNES, Scholar and Director LEIGHANNE OLSEN, Program Officer KATHERINE McCLURE, Senior Program Associate REBEKAH HUTTON, Research Associate PAMELA BERTELSON, Senior Program Assistant vii

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BOARD ON GLOBAL HEALTH1 RICHARD GUERRANT (Chair), Thomas H. Hunter Professor of International Medicine and Director, Center for Global Health, University of Virginia School of Medicine, Charlottesville, Virginia JO IVEY BOUFFORD (IOM Foreign Secretary), President, New York Academy of Medicine, New York, New York CLAIRE V. BROOME, Adjunct Professor, Division of Global Health, Rollins School of Public Health, Emory University, Atlanta, Georgia JACQUELYN C. CAMPBELL, Anna D. Wolf Chair, and Professor, Johns Hopkins University School of Nursing, Baltimore, Maryland THOMAS J. COATES, Michael and Sue Steinberg Professor of Global AIDS, Research Co-Director, UC Global Health Institute, David Geffen School of Medicine, University of California, Los Angeles, California GARY DARMSTADT, Director, Family Health Division, Global Health Program, Bill & Melinda Gates Foundation, Seattle, Washington VALENTIN FUSTER, Director, Wiener Cardiovascular Institute Kravis Cardiovascular Health Center Professor, Cardiology, Mount Sinai School of Medicine, Mount Sinai Medical Center, New York, New York JACOB A. GAYLE, Vice President, Community Affairs, Executive Director, Medtronic Foundation, Minneapolis, Minnesota GLENDA E. GRAY, Executive Director, Perinatal HIV Research Unit, Chris Hani Baragwanath Hospital, University of the Witwatersrand, Diepkloof, South Africa STEPHEN W. HARGARTEN, Professor and Chair, Emergency Medicine, Director, Medical College of Wisconsin, Milwaukee, Wisconsin JAMES HOSPEDALES, Coordinator, Chronic Disease Project, Health Surveillance and Disease Management Area, Pan American Health Organization and World Health Organization, Washington, DC PETER J. HOTEZ, Professor and Chair, Department of Microbiology, Immunology, and Tropical Medicine, The George Washington University, Washington, DC CLARION JOHNSON, Global Medical Director, Medicine and Occupational Medicine Department, Exxon Mobil, Fairfax, Virginia FITZHUGH MULLAN, Professor, Department of Health Policy, The George Washington University, Washington, DC OLUFUNMILAYO F. OLOPADE, Walter L. Palmer Distinguished Service Professor of Medicine, The University of Chicago, Chicago, Illinois 1 Institute of Medicine boards do not review or approve individual workshop summaries. The responsibility for the content of the workshop summary rests with the workshop rapporteurs and the institution. viii

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GUY PALMER, Regents Professor of Pathology and Infectious Diseases, Director of the School for Global Animal Health, Washington State University, Pullman, Washington THOMAS C. QUINN, Associate Director for International Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Professor of Medicine, International Health, Epidemiology, and Molecular Biology and Immunology, Johns Hopkins University School of Medicine, Baltimore, Maryland JENNIFER PRAH-RUGER, Associate Professor, Division of Health Policy and Administration, Yale University School of Public Health, New Haven, Connecticut Staff PATRICK KELLEY, Director ANGELA CHRISTIAN, Program Associate ix

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PLANNING COMMITTEE ON GLOBAL INFECTIOUS DISEASES AND FOOD SAFETY1 ROGER G. BREEZE, Lawrence Livermore National Laboratory, Livermore, California PETER DASZAK, EcoHealth Alliance, New York, New York DAVID L. HEYMANN, Health Protection Agency, London, United Kingdom JAMES M. HUGHES, Global Infectious Diseases Program, Emory University, Atlanta, Georgia GERALD T. KEUSCH, Boston University School of Medicine and Boston University School of Public Health, Boston, Massachusetts RIMA F. KHABBAZ, Centers for Disease Control and Prevention, Atlanta, Georgia LONNIE J. KING, The Ohio State University, Columbus, Ohio 1 Institute of Medicine planning committees are solely responsible for organizing the workshop, identifying topics, and choosing speakers. The responsibility for the published workshop summary rests solely with the workshop rapporteurs and the institution. x

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Reviewers This report has been reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise, in accordance with procedures approved by the National Research Council’s Report Review Committee. The purpose of this independent review is to provide candid and critical comments that will assist the institution in making its published report as sound as possible and to ensure that the report meets institutional standards for objectivity, evi- dence, and responsiveness to the study charge. The review comments and draft manuscript remain confidential to protect the integrity of the process. We wish to thank the following individuals for their review of this report: Roger G. Breeze, Lawrence Livermore National Laboratory, Livermore, California David Heymann, Health Protection Agency, London, United Kingdom James M. Hughes, Emory University, Atlanta, Georgia Stanley M. Lemon, University of North Carolina, Chapel Hill, North Carolina David Rizzo, University of California, Davis, California Jørgen Schlundt, Danish Technical University, Lyngby, Denmark Although the reviewers listed above have provided many constructive com- ments and suggestions, they did not see the final draft of the report before its release. The review of this report was overseen by Dr. Melvin Worth. Appointed by the Institute of Medicine, he was responsible for making certain that an inde- pendent examination of this report was carried out in accordance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content of this report rests entirely with the authors and the institution. xi

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Acknowledgments The Forum on Emerging Infections was created by the Institute of Medicine (IOM) in 1996 in response to a request from the Centers for Disease Control and Prevention (CDC) and the National Institutes of Health (NIH). The purpose of the Forum is to provide structured opportunities for leaders from government, academia, and industry to regularly meet and examine issues of shared concern regarding research, prevention, detection, and management of emerging, reemerg- ing, and novel infectious diseases in humans, plants, and animals. In pursuing this task, the Forum provides a venue to foster the exchange of information and ideas, identify areas in need of greater attention, clarify policy issues by enhanc- ing knowledge and identifying points of agreement, and inform decision makers about science and policy issues. The Forum seeks to illuminate issues rather than resolve them. For this reason, it does not provide advice or recommendations on any specific policy initiative pending before any agency or organization. Its value derives instead from the diversity of its membership and from the contributions that individual members make throughout the activities of the Forum. In Sep- tember 2003, the Forum changed its name to the Forum on Microbial Threats. The Forum on Microbial Threats and the IOM wish to express their warmest appreciation to the individuals and organizations who gave their valuable time to provide information and advice to the Forum through their participation in the planning and execution of this workshop. A full list of presenters, and their biographical information, may be found in Appendixes B and E, respectively. The Forum gratefully acknowledges the contributions of the members of the planning committee:1 Roger Breeze (Lawrence Livermore National Laboratory), 1 Institute of Medicine planning committees are solely responsible for organizing the workshop, identifying topics, and choosing speakers. The responsibility for the published workshop summary rests solely with the workshop rapporteurs and the institution. xiii

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xiv ACKNOWLEDGMENTS Peter Daszak (EcoHealth Alliance), David Heymann (Health Protection Agency), James Hughes (Emory University), Gerald Keusch (Boston University), Rima Khabbaz (Centers for Disease Control and Prevention), and Lonnie King (Ohio State University). The Forum is also indebted to the IOM staff who tirelessly contributed throughout the planning and execution of the workshop and the production of this workshop summary report. On behalf of the Forum, we gratefully acknowledge these efforts led by Dr. Eileen Choffnes, director of the Forum; Dr. LeighAnne Olsen, program officer; Katherine McClure, senior program associate; Rebekah Hutton, research associate; and Pamela Bertelson, senior program assistant, for dedicating much effort and time to developing this workshop’s agenda and for their thoughtful and insightful approach and skill in planning for the workshop and in translating the workshop’s proceedings and discussion into this workshop sum- mary report. We would also like to thank the following IOM staff and consultants for their valuable contributions to this activity: Daniel Bethea, Laura Harbold DeStefano, Alison Mack, Vilija Teel, and Sarah Ziegenhorn. Finally, the Forum wishes to recognize the sponsors that supported this activity. Financial support for this project was provided by the U.S. Department of Health and Human Services: NIH, National Institute of Allergy and Infectious Diseases, CDC, Food and Drug Administration, and the Fogarty International Center; Uniformed Services University of the Health Sciences; U.S. Depart- ment of Defense, Department of the Army: Global Emerging Infections Surveil- lance and Response System, Medical Research and Materiel Command, and the Defense Threat Reduction Agency; U.S. Department of Veterans Affairs; U.S. Department of Homeland Security; U.S. Agency for International Development; American Society for Microbiology; sanofi pasteur; Burroughs Wellcome Fund; GlaxoSmithKline; Infectious Diseases Society of America; and the Merck Com- pany Foundation. The views presented in this workshop summary are those of the workshop participants and have been summarized by the rapporteurs. They do not necessarily reflect the views of the Forum on Microbial Threats, its spon- sors, or the IOM.

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Contents Workshop Overview 1 Workshop Overview References, 103 Appendixes A Contributed Manuscripts, 115 A1 EHEC O104:H4 in Germany 2011: Large Outbreak of Bloody Diarrhea and Haemolytic Uraemic Syndrome by Shiga Toxin– Producing E. coli via Contaminated Food, 115 Reinhard Burger A2 One Health and Hotspots of Food-borne EIDs, 130 C. Zambrana-Torrelio, K. A. Murray, and P. Daszak A3 Plant Food Safety Issues: Linking Production Agriculture with One Health, 140 Marilyn C. Erickson and Michael P. Doyle A4 One Health and Food Safety—The Canadian Experience: A Holistic Approach Toward Enteric Bacterial Pathogens and Antimicrobial Resistance Surveillance, 176 Jane Parmley, Zee Leung, David Léger, Rita Finley, Rebecca Irwin, Katarina Pintar, Frank Pollari, Richard Reid-Smith, David Waltner-Toews, Mohamad Karmali, and Rainer Engelhardt A5 Overview of the Global Food System: Changes over Time/Space and Lessons for Future Food Safety, 189 Will Hueston and Anni McLeod xv

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xvi CONTENTS A6 The Australian Perspective, the Biosecurity Continuum from Preborder, to Border and Postborder, 198 Martyn Jeggo A7 Food Safety: A View from the Wild Side, 207 William B. Karesh, Elizabeth Loh, Catherine Machalaba A8 One Health and Food Safety, 218 Lonnie J. King A9 Food-borne Viruses from a Global Perspective, 225 Marion Koopmans A10 Microbe Hunting and Pathogen Discovery, 251 Nicole C. Arrigo and W. Ian Lipkin A11 Transmission of Human Infection with Nipah Virus, 271 Stephen P. Luby, Emily S. Gurley, and M. Jahangir Hossain A12 Date Palm Sap Linked to Nipah Virus Outbreak in Bangladesh, 2008, 283 Muhammad Aziz Rahman, Mohammad Jahangir Hossain, Sharmin Sultana, Nusrat Homaira, Salah Uddin Khan, Mahmudur Rahman, Emily S. Gurley, Pierre E. Rollin, Michael K. Lo, James A. Comer, Luis Lowe, Paul A. Rota, Thomas G. Ksiazek, Eben Kenah, Yushuf Sharker, and Stephen P. Luby A13 Food-borne Pathogen Control Programs, 298 Mike Robach A14 Emerging Food-borne Pathogens and Problems: Expanding Prevention Efforts Before Slaughter or Harvest, 307 Casey Barton Behravesh, Ian T. Williams, and Robert V. Tauxe A15 Antibiotic Resistance—Linking Human and Animal Health, 331 Henrik C. Wegener A16 Origins of Major Human Infectious Diseases, 349 Nathan D. Wolfe, Claire Panosian Dunavan, and Jared Diamond A17 The Outlook for Public Food Safety Research and USDA Science, 362 Catherine Woteki B Agenda 369 C Acronyms 373 D Glossary 377 E Speaker Biographies 385

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Tables, Figures, and Boxes TABLES WO-1 Understanding the One Health Paradigm for Food Safety, 16 WO-2 Many of the Major Food-Borne Pathogens in the United States Were Only Recently Characterized, 23 A3-1 Food-Borne Disease Outbreaks Attributed to a Single Commodity by Leading Food Vehicles, 2006-2008, 141 A3-2 Number of Outbreaks (illnesses) Reported Between 2000 and 2009 in the United States That Were Associated with Selected Fresh Produce Items as a Function of their Etiology, 142 A3-3 Selected Food-Borne Disease Outbreaks Attributed to Produce During the Period of 2006-2011, 144 A3-4 Prevalence of Salmonella in Lettuce, Cabbage, and Mixed Salads Throughout the World, 146 A3-5 Prevalence of Helminth and Protozoan Parasites in Leafy Greens from 2005 to 2010, 148 A3-6 Prevalence and Cell Numbers of Salmonella spp. in Manures from Domesticated Animals, 150 A3-7 Prevalence and Cell Numbers of Campylobacter spp. in Manures from Domesticated Animals, 152 A3-8 Prevalence and Cell Numbers of Shiga Toxin–Producing E. coli in Manures from Domesticated Animals, 153 A3-9 Prevalence and Cell Numbers of Cryptosporidium spp. in Manures from Domesticated Animals, 157 xvii

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xviii TABLES, FIGURES, AND BOXES A3-10 Prevalence of Salmonella spp., STEC, and Protozoan Parasites in Environmental Waters, 159 A3-11 Prevalence of Enteric Food-Borne Pathogens in Wildlife and Insects, 163 A6-1 Major Differences to Risk Management of Infectious Diseases Versus Those Associated with Food Safety Issues, 201 A12-1 Profiles of the Case-Patients in February 2008 Nipah Outbreaks, Manikgonj and Rajbari Districts, Bangladesh, 290 A12-2 Laboratory Results of Case-Patients in February 2008, Manikgonj and Rajbari Districts, Bangladesh, 290 A12-3 Nucleotide Differences Between Nipah Virus Isolated from Bangladesh (2004, 2008) and India (2007), 292 A12-4 Bivariate Analysis of Exposures for Nipah Virus Infection in February 2008, Manikgonj and Rahbari Districts, Bangladesh, 293 A14-1 Major Pathogens Identified as Foodborne Since 1970, 309 A14-2 Major Food-Animal Reservoirs for Human Foodborne Bacterial Pathogens, 310 A14-3 Fifteen New Food Vehicles Identified from 2006 Through March 2012 in Foodborne Outbreaks Affecting the United States, 311 FIGURES WO-1 The well-traveled salad, 2 WO-2 U.S. agricultural and seafood imports (millions of U.S. dollars), 8 WO-3 The convergence model, 10 WO-4 Trends in global population: 1950-2015, 12 WO-5 World meat consumption, 1983-2020, 13 WO-6 Why diseases emerge, 14 WO-7 Global supply chain complexity: Origin and contents of a generic “megaburger,” 19 WO-8 The global U.S. food supply: Many components, 20 WO-2-1 Scanning electron microscope image shows the characteristic spiral, or corkscrew, shape of Campylobacter jejuni cells, 24 WO-2-2 Clostridium perfringens bacterium. Colored TEM. Magnification: 43,000x, 25 WO-2-3 This colorized scanning electron micrograph (SEM) depicts a number of Escherichia coli bacteria of the strain O157:H7 (Magnification: 6,836), 26 WO-2-4 False-color transmission electron micrograph (TEM) of a single flagellate bacterium, Listeria monocytogenes, 27

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xix TABLES, FIGURES, AND BOXES WO-2-5 Transmission electron micrograph of norovirus virions, 28 WO-2-6 Negatively color-enhanced scanning electron micrograph showing Salmonella typhimurium (red) invading cultured human cells, 29 WO-2-7 Colored transmission electron micrograph (TEM) of Toxoplasma gondii parasites, cause of toxoplasmosis, 30 WO-9 The true burden of food-borne disease remains unknown, 31 WO-10 Many different pathogens and toxins, 33 WO-11 Foods implicated in outbreaks, 33 WO-3-1 Aerial (~15 km2) photograph of ranch A showing overlapping circular buffer regions around feral swine trap 1 and trap 2 (San Benito crop year 2006; Image Trader, Flagstaff, AZ), 38 WO-3-2 Incidence of HUS, 39 WO-3-3 Persons infected with the outbreak-associated strains of Listeria monocytogenes, by state, 41 WO-3-4 Cruise ships provide ideal conditions for the amplification and spread of infectious diseases, 43 WO-12 Fifteen years of progress in prevention: Trends in food-borne diseases, Foodnet, 1996-2010, 45 WO-13 EHEC outbreak 2011: Investigation of the outbreak along the food chain, 49 WO-14 Malaysia Nipah outbreak, 50 WO-15 Date palm sap collection, 51 WO-16 How often do bats visit date palm trees to drink their sap?, 52 WO-17 Bacteria manipulate leaf stomata and get inside, 59 WO-18 Grouping of (potential) food-borne viruses, 60 WO-19 Pyramids and snowball effects, 63 WO-20 DANMAP: Integrated surveillance of antimicrobial resistance and antimicrobial usage in Denmark, 64 WO-21 A schematic representation of how farm size can affect risk of avian influenza emergence, 68 WO-22 Hotspots for food-borne pathogen emergence, 70 WO-23 John Snow’s map of the 1854 cholera epidemic in London, 73 WO-24 Human viruses have animal origins, 74 WO-25 A staged strategy for pathogen discovery, 77 WO-26 A One Health approach recognizes the interconnection between humans, plants, animals, water, and the environment as it relates to health problems, 82 WO-27 The “host–parasite” continuum, 83 WO-28 Schematic presentation of the collection, collation, analysis, and interpretation of surveillance data and the subsequent dissemination of information to all the major stakeholders in food safety, 87 WO-29 Global-to-local food safety systems, 96

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xx TABLES, FIGURES, AND BOXES A1-1 Total number of EHEC and HUS cases and associated deaths during the outbreak of EHEC O104:H4 in summer 2011 in Germany and comparison to an average year, 117 A1-2 Epidemiological curve of EHEC and HUS cases and overview of epidemiological studies performed by the Robert Koch Institute for identification of sprouts as the vehicle of transmission, 118 A1-3 Recipe-based restaurant cohort study of the Robert Koch Institute reveals risk for infection associated with the consumption of sprouts, 120 A1-4 Trading network reveals linkage of 41 identified outbreak clusters, 121 A1-5 Electron micrograph of EHEC O104:H4, 123 A1-6 Putative origin of the EHEC outbreak strain as a combination of viru - lence traits derived from two different ancestors, 124 A2-1 Proportion of EID events categorized by transmission mode, 131 A2-2 Number of EID events per transmission mode classified by pathogen type, 134 A2-3 Number of EID events per transmission mode categorized by zoonotic origin, 135 A2-4 Proportion of drug-resistant and nonresistant EID events of zoonotic or nonzoonotic origin, 136 A2-5 Association of food-borne EIDs with other drivers, 137 A2-6 Relative risk of food-borne EID events, based on Jones et al. (2008), 138 A4-1 Economic impact examples, 178 A4-2 Transfer model for antimicrobial resistance genes, 180 A4-3 The intersection of enteric agents, animals and humans, and the environmental factors that influence the occurrence of zoonotic bacterial infections and the emergence of AMR, 182 A4-4 Ceftiofur resistance in E. coli from retail chicken and S. Heidelberg from retail chicken and humans, CIPARS 2003-2010, 186 A5-1 Global supply chain complexity. Movement of commodities, 192 A5-2 Global supply chain complexity. Ingredient list, 193 A5-3 Globalizing the cheeseburger, 194 A6-1 When to act: Generalized invasion curve showing actions appropriate to each stage, 202 A7-1 The number of infectious disease events that emerged from wildlife between 1940 and 2004 as published by Jones et al. (2008), 208 A7-2 All food-borne EID events from 1940-2004 (n = 100), broken down by zoonotic versus nonzoonotic origin, 209

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xxi TABLES, FIGURES, AND BOXES A7-3 All food-borne emerging infectious diseases from 1940 to 2004 (n = 100) with their respective “drivers of emergence” as published by Jones et al. (2008), 209 A7-4 Routes of contamination resulting in food-borne illness linked to wildlife, 211 A9-1 Epidemiology of food- and water-borne viruses, showing complexity of transmission and possible sources of infection, 226 A9-2 Steps required and common challenges for establishing proof of food- borne (viral) infection, 236 A10-1 Growth of the viral sequence database mapped to seminal discoveries and improvements in sequencing technology, 254 A10-2 Staged strategy for pathogen discovery and link to causation. In the molecular era of pathogen discovery, culture and molecular methods are pursued in parallel until an agent is detected, isolated, and characterized, 263 A11-1 Range of Pteropus bats based on RM Nowak, 273 A11-2 Chain of person to person transmission in Nipah outbreak, Faridpur, Bangladesh, 2004, 276 A12-1 Bangladesh map showing location of Nipah surveillance sites, previous Nipah outbreak areas, and February 2008 outbreak areas of Bangladesh, 285 A12-2 Date of illness onset from both clusters occurred over 6 days during February 2008, Manikgonj and Rajbari Districts, Bangladesh, 287 A13-1 Roadmap for the components of global food safety, 300 A13-2 Cargill food safety policy, 303 A13-3 Corporate food safety and regulatory affairs, 304 A13-4 Cargill environmental monitoring decision tree, 306 A14-1 The food production chain from the farm to the table, 308 A14-2 Distribution of illnesses by food type in 1,565 foodborne outbreaks caused by a single food type and reported to CDC’s National Foodborne Disease Outbreak Surveillance System, 2003-2008, 311 A14-3 Relative rates of laboratory-confirmed infections with Campylobacter, Shiga toxin–producing Escherichia coli O157, Listeria, Salmonella, and Vibrio, compared with 1996-1998 rates, by year, in the United States during 1996-2010, based on data from the Foodborne Diseases Active Surveillance Network (FoodNet), 312

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xxii TABLES, FIGURES, AND BOXES A14-4 Number of reported cases of salmonellosis, by serotype, England and Wales, 2000-2010, 317 A15-1 The epidemiology of antimicrobial resistance at the human–animal interface is invariably complex, 333 A15-2 Flow of samples, isolates, and data in the Danish Integrated Antimicrobial Resistance and Antimicrobial Usage Monitoring Programme—DANMAP, 338 A15-3 Comparison of the sales of veterinary antibacterial agents between 10 European countries (mg per kg meat produced), 339 A15-4 The total consumption of fluoroquinolones in Danish food-animal production, following voluntary and regulatory efforts to reduce the amounts used in 1999 and 2002, respectively, 342 A15-5 Resistance (%) to erythromycin among Enterococcus faecium and Enterococcus faecalis from swine and the consumption of macrolides in swine, Denmark, 343 A15-6 Resistance (%) to vancomycin in Enterococcus faecium from broilers and the consumption of avoparcin, Denmark, 344 A15-7 Prevalence of ceftiofur resistance (moving average of the current quarter and the previous two quarters) among retail chicken Escherichia coli, and retail chicken and human clinical Salmonella enterica serovar Heidelberg isolates during 2003-2008 in Québec, 345 A15-8 Sales of antimicrobials for therapeutic use in farmed fish in Norway versus produced biomass, 346 A16-1 Illustration of the five stages through which pathogens of animals evolve to cause diseases confined to humans, 352 BOXES WO-1 Wicked Problems, 14 WO-2 The Seven Most Common Food-Borne Pathogens in the United States, 24 WO-3 Recent Food-borne Outbreaks: The Changing Nature of the “Threat,” 36 WO-4 Molecular Methods for Pathogen Discovery, 78 A16-1 Five Stages Leading to Endemic Human Diseases, 351 A16-2 Transitions Between Stages, 353