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THE DOMESTIC AND INTERNATIONAL IMPACTS OF THE 2009-H1N1 INFLUENZA A PANDEMIC

Global Challenges, Global Solutions

Workshop Summary

David A. Relman, Eileen R. Choffnes, and Alison Mack, Rapporteurs

Forum on Microbial Threats

Board on Global Health

INSTITUTE OF MEDICINE
OF THE NATIONAL ACADEMIES

THE NATIONAL ACADEMIES PRESS

Washington, D.C.
www.nap.edu



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David A. Relman, Eileen R. Choffnes, and Alison Mack, Rapporteurs Forum on Microbial Threats Board on Global Health

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THE NATIONAL ACADEMIES PRESS 500 Fifth Street, N.W. 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. This project was supported by contracts between the National Academy of Sciences and the U.S. Department of Health and Human Services: National Institutes of Health, National Institute of Allergy and Infectious Diseases, Centers for Disease Control and Prevention, and Food and Drug Administration; U.S. Department of Defense, Department of the Army: Global Emerging Infections Surveillance and Response System, Medical Research and Materiel Command, and 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; Pfizer; GlaxoSmithKline; Infectious Diseases Society of America; and the Merck Company Foundation. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the organizations or agencies that provided support for this project. International Standard Book Number-13: 978-0-309-14677-7 International Standard Book Number-10: 0-309-14677-1 Additional copies of this report are available from the National Academies Press, 500 Fifth Street, N.W., Lockbox 285, Washington, DC 20055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet, http://www.nap.edu. For more information about the Institute of Medicine, visit the IOM home page at: www. iom.edu. Copyright 2010 by the National Academy of Sciences. All rights reserved. Printed in the United States of America 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. Cover image: A stained glass window 21″ × 56″ depicting the natural history of influenza viruses and zoonotic exchange in the emergence of new strains is shown in reduced size. Based on the work done at St. Jude Children’s Research Hospital supported by American Lebanese Syrian Associated Charities and the National Institute of Allergy and Infec- tious Diseases. Artist: Jenny Hammond, Highgreenleycleugh, Northumberland, England. Commissioned by Rob and Marjorie Webster. Suggested citation: IOM (Institute of Medicine). 2010. The domestic and international impacts of the 2009-H1N1 influenza A pandemic: Global challenges, global solutions . 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 man- date 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 examination 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 National 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 THREATS DAVID A. RELMAN (Chair), Stanford University and VA Palo Alto Health Care System, Palo Alto, California JAMES M. HUGHES (Vice Chair), Global Infectious Diseases Program, Emory University, Atlanta, Georgia RUTH L. BERKELMAN, Emory University, Center for Public Health Preparedness and Research, Rollins School of Public Health, Atlanta, Georgia ENRIQUETA C. BOND, Consultant, Marshall, Virginia ROGER G. BREEZE, Centaur Science Group, Washington, DC STEVEN J. BRICKNER, SJ Consulting, LLC, Ledyard, Connecticut JOHN E. BURRIS, Burroughs Wellcome Fund, Research Triangle Park, North Carolina GAIL H. CASSELL, Eli Lilly & Company, Indianapolis, Indiana MARK B. FEINBERG, Merck Vaccine Division, Merck & Co., West Point, Pennsylvania DARRELL R. GALLOWAY, Medical S&T Division, Defense Threat Reduction Agency, Fort Belvoir, Virginia S. ELIZABETH GEORGE, Biological and Chemical Countermeasures Program, Department of Homeland Security, Washington, DC JESSE L. GOODMAN, Center for Biologics Evaluation and Research, Food and Drug Administration, Rockville, Maryland EDUARDO GOTUZZO, Instituto de Medicina Tropical–Alexander von Humbolt, Universidad Peruana Cayetano Heredia, Lima, Peru JO HANDELSMAN, College of Agricultural and Life Sciences, University of Wisconsin, Madison CAROLE A. HEILMAN, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland DAVID L. HEYMANN, Health Protection Agency, London, UK PHIL HOSBACH, Sanofi Pasteur, Swiftwater, Pennsylvania STEPHEN A. JOHNSTON, Arizona BioDesign Institute, Arizona State University, Tempe KENT KESTER, Walter Reed Army Institute of Research, Silver Spring, Maryland GERALD T. KEUSCH, Boston University School of Medicine and Boston University School of Public Health, Massachusetts RIMA F. KHABBAZ, Centers for Disease Control and Prevention, Atlanta, Georgia IOM Forums and Roundtables do not issue, review, or approve individual documents. The responsibility for the published workshop summary rests with the workshop rapporteur(s) and the institution. v

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LONNIE J. KING, Ohio State University, Columbus, Ohio STANLEY M. LEMON, School of Medicine, University of Texas Medical Branch, Galveston EDWARD McSWEEGAN, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland PAUL F. MILLER, Pfizer, Groton, Connecticut STEPHEN S. MORSE, Center for Public Health Preparedness, Columbia University, New York MICHAEL T. OSTERHOLM, Center for Infectious Disease Research and Policy, School of Public Health, University of Minnesota, Minneapolis GEORGE POSTE, Complex Adaptive Systems Initiative, Arizona State University, Tempe JOHN C. POTTAGE, JR., GlaxoSmithKline, Collegeville, Pennsylvania GARY A. ROSELLE, Veterans Health Administration, Department of Veterans Affairs, Washington, DC KEVIN RUSSELL, Global Emerging Infections Surveillance and Response System, Department of Defense, Silver Spring, Maryland JANET SHOEMAKER, American Society for Microbiology, Washington, DC P. FREDERICK SPARLING, University of North Carolina, Chapel Hill TERENCE TAYLOR, International Council for the Life Sciences, Washington, DC MURRAY TROSTLE, U.S. Agency for International Development, Washington, DC Staff EILEEN CHOFFNES, Director KATE SKOCZDOPOLE, Senior Program Associate KATHLEEN C. OSTAPKOVICH, Research Associate (until October 2009) KENISHA PETERS, Senior Program Assistant (until August 2009) ROBERT GASIOR, Senior Program Assistant (from September 2009) ALISON MACK, Science Writer vi

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BOARD ON GLOBAL HEALTH Richard Guerrant (Chair), Thomas H. Hunter Professor of International Medicine and Director, Center for Global Health, University of Virginia School of Medicine, Charlottesville Jo Ivey Boufford (IOM Foreign Secretary), President, New York Academy of Medicine, New York Claire V. Broome, Adjunct Professor, Division of Global Health, Rollins School of Public Health, Emory University Jacquelyn C. Campbell, Anna D. Wolf Chair, and Professor, Johns Hopkins University School of Nursing, Baltimore, Maryland Thomas J. Coates, Professor, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California 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 Sue Goldie, Associate Professor of Health Decision Science, Department of Health Policy and Management, Center for Risk Analysis, Harvard University School of Public Health, Boston, Massachusetts Peter J. Hotez, Professor and Chair, Department of Microbiology, Immunology, and Tropical Medicine, The George Washington University, Washington, DC Gerald T. Keusch, Assistant Provost for Global Health, Boston University School of Medicine, and Associate Dean for Global Health, Boston University School of Public Health, Massachusetts Michael Merson, Director, Duke Global Health Institute, Duke University, Durham, North Carolina Fitzhugh Mullan, Professor, Department of Health Policy, George Washington University, Washington, DC Philip Russell, Professor Emeritus, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland Staff Patrick Kelley, Director Allison Brantley, Senior Program Assistant (until November 2009) Angela Mensah, Program Associate IOM boards do not review or approve individual reports and are not asked to endorse conclusions and recommendations. The responsibility for the content of the report rests with the authors and the institution. vii

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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 Breeze, Centaur Science Group John Pottage, Infectious Disease Medicine Development Center, GlaxoSmithKline P. Frederick Sparling, School of Medicine, University of North Carolina Mary Wilson, Department of Population and International Health, Harvard University Although the reviewers listed above have provided many constructive com- ments and suggestions, they were not asked to endorse 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 independent 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 authoring committee and the institution. ix

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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 meet and examine issues of shared concern regarding research, prevention, detection, and management of emerging or reemerging infectious diseases. 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 enhancing knowledge and identifying points of agree- ment, 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 September 2003, the Forum changed its name to the Forum on Microbial Threats. The Forum on Microbial Threats, and the IOM, wish to express their warm- est appreciation to the individuals and organizations who gave their valuable time to provide information and advice to the Forum through their participation in this workshop. A full list of presenters may be found in Appendix A. The Forum is indebted to the IOM staff who contributed during the course of the workshop and the production of this workshop summary. On behalf of the Forum, we gratefully acknowledge the efforts led by Dr. Eileen Choffnes, director of the Forum; Kate Skoczdopole, senior program associate; K. C. Ostapkovich, research associate; Kenisha Peters, senior program assistant; and Robert Gasior, xi

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xii ACKNOWLEDGMENTS 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 dis- cussion into this workshop summary. We would also like to thank the following IOM staff and consultants for their valuable contributions to this activity: Alison Mack, Jordan Wyndelts, Jill Grady, Jackie Turner, and Heather Phillips. Finally, the Forum wishes to recognize the sponsors that supported this activ- ity. Financial support for this project was provided by the U.S. Department of Health and Human Services: National Institutes of Health, National Institute of Allergy and Infectious Diseases, Centers for Disease Control and Prevention, and Food and Drug Administration; U.S. Department of Defense, Department of the Army: Global Emerging Infections Surveillance and Response System, Medical Research and Materiel Command, and 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; Pfizer; GlaxoSmithKline; Infectious Diseases Society of America; and the Merck Company Foundation. The views presented in this workshop summary report are those of the workshop participants and rapporteurs and are not necessarily those of the Forum on Microbial Threats or its sponsors.

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Contents Workshop Overview 1 Organization of the Workshop Summary, 3 2009-H1N1 Influenza A in Context, 3 Characterizing the Virus, 18 The Pandemic’s Progress, 29 The Scientific Response, 51 The Public Health Response, 66 Workshop Overview References, 85 Appendixes A Contributed Manuscripts, 95 A1 Technical Report for State and Local Public Health Officials and School Administrators on CDC Guidance for School (K-12) Responses to Influenza during the 2009-2010 School Year, 95 CDC Community Mitigation Task Force A2 Predicting Emerging Diseases in the Twenty-first Century: The Case of Zoonotic Influenza, 111 Kurt J. Vandegrift, Parviez Hosseini, Ph.D., and Peter Daszak, Ph.D. A3 The Spring 2009 Influenza A H1N1 Outbreak: A Local Public Health Perspective, 120 Jeffrey S. Duchin, M.D. xiii

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xiv CONTENTS A4 International Law and Equitable Access to Vaccines and Antivirals in the Context of 2009-H1N1 Influenza, 137 David P. Fidler, J.D. A5 In Vitro and In Vivo Characterization of New Swine-Origin H1N1 Influenza Viruses, 155 Yasushi Itoh, Kyoko Shinya, Maki Kiso, Tokiko Watanabe, Yoshihiro Sakoda, Masato Hatta, Yukiko Murramoto, Daisuke Tamura, Yuko Sakai-Tagawa, Takeshi Noda, Saori Sakabe, Masaki Imai, Yasuko Hatta, Shinji Watanabe, Chengjun Li, Shinya Yamada, Ken Fujii, Shin Murakami, Hirotaka Imai, Satoshi Kakugawa, Mutsumi Ito, Ryo Takano, Kiyoko Iwatsuki-Horimoto, Masayuki Shinmojima, Taisuke Horimoto, Hideo Goto, Kei Takahashi, Akiko Makino, Hirohito Ishigaki, Misako Nakayama, Masatoshi Okamatsu, Kazuo Takahashi, David Warshauer, Peter A. Shult, Reiko Saito, Hiroshi Suzuki, Yousuke Furuta, Makoto Yamashita, Keiko Mitamura, Kunio Nakano, Morio Nakamura, Rebecca Brockman-Schneider, Hiroshi Mitamura, Masahiko Yamazaki, Norio Sugaya, M. Suresh, Makoto Ozawa, Gabriele Neumann, James Gern, Hiroshi Kida, Kazumasa Ogasawara, and Yoshihiro Kawaoka1 Supplementary Information, 173 A6 Estimation of the Reproductive Number and the Serial Interval in Early Phase of the 2009 Influenza A⁄H1N1 Pandemic in the USA, 191 Laura Forsberg White, Jacco Wallinga, Lyn Finelli, Carrie Reed, Steven Riley, Marc Lipsitch,2 and Marcello Pagano A7 The Severity of Pandemic H1N1 Influenza in the United States, from April to July 2009: A Bayesian Analysis, 208 Anne M. Presanis, Daniela De Angelis, The New York City Swine Flu Investigation Team, Angela Hagy, Carrie Reed, Steven Riley, Ben S. Cooper, Lyn Finelli, Paul Biedrzycki, and Marc Lipsitch 2 Text S1 Supplementary Methods, 234 A8 Hard Choices in Difficult Situations: Ethical Issues in Public Health Emergencies, 248 Bernard Lo, M.D. A9 Rumors of Pandemic: Monitoring Emerging Disease Outbreaks on the Internet, 269 Lawrence C. Madoff, M.D., and John Brownstein, Ph.D. 1 Dr. Kawaoka was a speaker at the workshop. 2 Dr. Lipsitch was a speaker at the workshop.

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xv CONTENTS A10 Preliminary Observation of the Epidemiology of Seasonal and Pandemic Influenza A (H1N1) in South Africa, 2009, 283 B. D. Schoub, M.D., D.Sc., F.R.C.Path., B. N. Archer, B.Med., M.P.H., C. Cohen, M.Sc., M.B.B.Ch., F.C.Path., D. Naidoo, M.Sc., J. Thomas, M.B.B.Ch., F.C.Path., C. Makunga, B.Sc.Hons., M.B.B.Ch., M. Venter, Ph.D., G. Timothy, M.B.B.Ch., A. Puren, Ph.D., M.B.B.Ch., J. McAnerney, R.N., A. Cengimbo, M.B.B.Ch., and L. Blumberg, M.B.B.Ch., M.Med. A11 Reflections on the 1976 Swine Flu Vaccination Program, 297 David J. Sencer and J. Donald Millar A12 Southern Hemisphere, Northern Hemisphere: A Global Influenza World, 306 Kennedy F. Shortridge, Ph.D. A13 Influenza (H1N1) Pandemic 2009, 327 Osvaldo Uez, Karina Balbuena, Martina Iglesias, María del Carmen Weis, Christian Hertlein, Ana Balanzat, Cora Santandrea, Sebastián Genero, Teresa Varela, Alicia Manana, Claudia Ling, Luis Carlino A14 Origins and Evolutionary Genomics of the 2009 Swine-Origin H1N1 Influenza A Epidemic, 342 Gavin J. D. Smith, Dhanasekaran Vijaykrishna, Justin Bahl, Samantha J. Lycett, Michael Worobey,3 Oliver G. Pybus, Siu Kit Ma, Chung Lam Cheung, Jayna Raghwani, Samir Bhatt, J. S. Malik Peiris, Yi Guan, and Andrew Rambaut Supplementary Information, 354 B Agenda 381 C Acronyms 386 D Glossary 389 E Forum Member Biographies 397 3 Dr. Worobey was a speaker at the workshop.

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Tables, Figures, and Boxes TABLES WO-1 Mortality Associated with Influenza Pandemics and Selected Seasonal Epidemic Events, 1918-2009, 8 WO-2 Age-Specific Severity Estimates, 63 A4-1 Overview of Resource Mobilization (millions), 151 A5-1 Virus Titres in Organs of Infected Cynomolgus Macaques, 159 A5-2 Virus Titres in Organs of Infected Mice, 186 A5-3 Virus Titres in Respiratory Swabs from Infected Cynomolgus Macaques, 186 A5-4 Virus Titres in Respiratory Organs of Infected Ferrets, 187 A5-5 Virus Titres in Nasal Swabs of Inoculated and Contact Ferrets, 188 A5-6 Virus Titres in Organs of Infected Miniature Pigs, 189 A5-7 Virus Titres in Nasal Swabs from Infected Miniature Pigs, 189 A5-8 Virus Susceptibility to Antiviral Compounds in Cell Culture, 190 A5-9 Virus Sensitivity in Neuraminidase Assays, 190 A6-1 Estimates Obtained from the Original, Imputed, and Augmented Data, 199 A6-2 Estimates of the Reproductive Number the Mean of the Serial Interval (SI) Is 3.6 Days with SD of 1.6 Days (Cowling et al., 2009) or Mean of 1.91 Days and SD of 1 Days (Fraser et al., 2009), 203 A7-1 Detection Probabilities and Their Prior Distributions, 217 A7-2 Cases at Each Level of Severity, 220 xvi

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xvii TABLES, FIGURES, AND BOXES A7-3 Posterior Median (95% CI) Estimates of the sCFR, sCIR, and sCHR, by Age Group, Based on a Combination of Data from New York City and Milwaukee, and Survey Data on the Frequency of Medical Attendance for Symptomatic Cases, 221 A7-4 Posterior Median (95% CI) Estimates of the sCFR, sCIR, and sCHR by Age Group, Using Self-Reported ILI as the Denominator of Symptomatic Cases, 222 A8-1 Ethical Considerations During a Declared Public Health Emergency, 252 A10-1 First Confirmed Cases of 2009-H1N1 Influenza A, 287 A10-2 Travel History of 42 Cases Within the First 100 Investigated, 288 A10-3 Laboratory-Confirmed Pandemic 2009-H1N1 Influenza A Cases by Province, South Africa, as of December 15, 2009, 290 A10-4 Pandemic 2009-H1N1 Influenza A Cases by Age Group, South Africa, as of December 15, 2009, 291 A10-5 Breakdown of First 100 Cases by Race, 293 A12-1 China H1N1—Then and Now, 308 A12-2 Deaths Due to Influenza in Hong Kong for Each Month from 1918-1928, 308 A12-3 Respiratory Pathogens Isolated in Hong Kong at Selected Times During the 2009-H1N1 Influenza A Outbreak, 313 A12-4 Some Areas for Investigation, 315 A13-1 Underlying Conditions Present by Age Group, 340 A14-1 Time of Most Recent Common Ancestors for the S-OIV Outbreak, 346 A14-2 SLAC Results, 374 A14-3 SNAP Results, 374 A14-4 Hong Kong Swine Genetic Origins, 375 A14-5 S-OIV Sequences Available on NCBI Influenza Virus Database at the Time of Analysis, 376 FIGURES WO-1 Host cell invasion and replication by the influenza virus, 7 WO-2 Genetic relationships among human and relevant swine influenza viruses, 1918-2009, 9 WO-3 The rate of globalization has accelerated to the point where we are connected as never before via globalized travel and trade networks, 16 WO-4 Reconstruction of the sequence of reassortment events leading up to the emergence of S-OIV, 20 WO-5 Lung tissues infected with 2009-H1N1 influenza A, 23

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xviii TABLES, FIGURES, AND BOXES WO-6 Spherical viral particles typical of seasonal H1N1 influenza, and the filamentous 2009-H1N1 influenza A, 24 WO-7 Virus transmission from infected ferrets to those in adjacent cages, 25 WO-8 Pathological examination of the lungs of infected cynomolgus macaques, 26 WO-9 Neutralization activities in human sera against viruses, 27 WO-10 CA04 sensitivity to antiviral compounds in mice, 30 WO-11 2009-H1N1 influenza A pandemic laboratory-confirmed cases and cumulative number of deaths as reported to WHO as of March 7, 2010, 31 WO-12 Number of specimens positive for influenza by subtype, Northern Hemisphere, April 19 to August 29, 2009, 35 WO-13 Number of specimens positive for influenza by subtypes, Southern Hemisphere, April 19 to August 29, 2009, 36 WO-14 Number of specimens positive for influenza by subtype, Chile, 37 WO-15 Number of specimens positive for influenza by subtype, Australia, 38 WO-16 Number of specimens positive for influenza by subtype, Hong Kong, 39 WO-17 Number of specimens positive for influenza by subtype, Cambodia, 40 WO-18 Number of specimens positive for influenza by subtype, Kenya, 41 WO-19 Influenza viral watch sentinel surveillance, update to end of week 35 (week ending August 30, 2009), 42 WO-20 Total influenza viruses from sentinel surveillance by type and week reported to August 23, 2009, and the total percentage positive from the swabs received, New Zealand, 43 WO-21 Percentage of visits for ILI reported by the U.S. Outpatient ILI Surveillance Network (ILINet) weekly national summary, October 1, 2006 to February 27, 2010, 44 WO-22 Epidemic curve in Mexico, cumulative through early September 2009, 45 WO-23 Viral shedding prior to and following treatment, 46 WO-24 Confirmed 2009-H1N1 influenza A cases in Peru, 2009, 47 WO-25 The long tradition of pigs and poultry sharing human dwellings in China, 50 WO-26 Spatial pattern in emerging infectious disease events, 59 WO-27 The pandemic severity scale developed by the U.S. government for planning and response, 61 WO-28 Severity pyramid, 62

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xix TABLES, FIGURES, AND BOXES A2-1 Chicken: a growth category, 117 A3-1 Laboratory-confirmed 2009-H1N1 influenza A infections by age, April-July 2009, King County, Washington, 121 A3-2 Emergency department visits for influenza-like illness, January 1, 2009 through June 20, 2009, King County, Washington, 121 A5-1 Pathological examination of the lungs of infected cynomolgus macaques, 160 A5-2 CA04 sensitivity to antiviral compounds in mice, 162 A5-3 Neutralization activities in human sera against viruses, 164 A5-4 Growth properties of viruses in cells, 173 A5-5 Morphology of budding CA04 virions, 174 A5-6 Body weight changes in infected mice, 176 A5-7 Pathological findings in infected mice, 177 A5-8 Pro-inflammatory cytokine/chemokine responses in the lungs of infected mice, 178 A5-9 Body temperatures of infected cynomolgus macaques, 180 A5-10 Pathological findings in infected cynomolgus macaques, 181 A5-11 Detection of viral antigens in type II pneumocytes in the lungs of CA04-infected cynomolgus macaques, 182 A5-12 Pro-inflammatory cytokine/chemokine responses in the lungs of infected cynomolgus macaques, 183 A5-13 Pathological findings in infected ferrets, 184 A5-14 Pathological findings in infected miniature pigs, 185 A6-1 Confirmed and probable cases in the United States plotted by onset time, 195 A6-2 (A) Reporting delay by the date of report. (B) Imputed data and original data. (C) All data (right frame), (D) only augmented data where at least 5% of the data is observed, 197 A6-3 Serial interval estimates for k = 4, 5, 6, and 7 days with –log(likelihood) values, 198 A6-4 Estimates for the reproductive number, mean, and variance of the serial interval, 200 A6-5 Serial interval estimate using data up to and including 4/25/2009 (top figure), 4/26/2009 (second), 4/27/2009 (third), and 4/28/2009 (bottom figure), 201 A7-1 Diagram of two approaches to estimating the sCFR, 213 A7-2 Schematic illustration of the relationship between the observed data (rectangles) and the conditional probabilities (blue circles), 216 A7-3 Assumed severity hierarchy, 237 A7-4 Simplified directed acyclic graph displaying the dependencies in part of the model, 239 A7-5 Prior versus posterior number of symptomatic infections, Approach 1, 246

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xx TABLES, FIGURES, AND BOXES A7-6 Prior vs posterior number of symptomatic infections, by age, Approach 1, 247 A9-1 Hierarchichal nature of traditional public health reporting, 272 A9-2 Informal-source surveillance, 273 A9-3 HealthMap screen shot, 275 A9-4 Google Flu Trends screen shot, 276 A9-5 Quantitation of subjects in ProMED reports from 1996-2008, 279 A9-6 Timeline showing time differences between official WHO reports, selected informal reports, and various “outbreak milestones,” 281 A10-1 Influenza results by type and subtype: South Africa 2005-2008, 285 A10-2 Onset and duration of influenza season, 1985-2007, 286 A10-3 Influenza strains detected, South Africa, 1984-2008, 286 A10-4 Epidemic curve of laboratory-confirmed pandemic 2009-H1N1 influenza A cases and deaths by week, South Africa, as of December 15, 2009 (n[cases]=12,683), 287 A10-5 Positive samples by influenza types and subtype: Viral Watch South Africa 2009, 289 A10-6 Severe acute respiratory illness (SARI) surveillance: respiratory virus report, 289 A10-7 Number of laboratory confirmed pandemic 2009-H1N1 influenza A cases by age group, as of December 15, 2009 (n = 11,729), 291 A10-8 Age distribution of patients with seasonal A H3N2 and pandemic 2009-H1N1 influenza A, 292 A10-9 Age distribution of patients with seasonal A H1N1 (2008) and pandemic 2009-H1N1 influenza A, 292 A10-10 Age distribution of patients with influenza B and pandemic 2009- H1N1 influenza A, 293 A10-11 Reported symptoms in first 100 confirmed cases, South Africa, 294 A12-1 General patterns of temporal occurrence of influenza A and B viruses in eastern Asia and Australasia, 310 A12-2 Long-term steps for the prevention of influenza pandemics, 319 A12-3 Emphasizing the need for increasing influenza virus surveillance for the prevention of pandemic influenza, 320 A12-4 Toward a unified, global effort for the prevention of pandemic influenza, 321 A12-5 Fundamental principles still apply, 322 A13-1 Cases of 2009-H1N1 influenza A by date of onset of symptoms, April-May 2009, Argentina (n = 250), 328 A13-2 Distribution of confirmed cases by date of onset of symptoms (n = 99), 328 A13-3 Temporal presentation of cases and contacts in the school population under study, May 16-31, 2009 (n = 102), 329 A13-4 Affected schools, May 2009, 330

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xxi TABLES, FIGURES, AND BOXES A13-5 Distribution of confirmed cases and cases under study by age and date of onset of symptoms, city of Buenos Aires and Province of Buenos Aires, April-July 2009 (n = 5,145), 331 A13-6 Distribution of confirmed cases and cases under study by age and date of onset of symptoms, rest of country (except Buenos Aires and Province of Buenos Aires), April-July 2009 (n = 5,030), 331 A13-7 Distribution of confirmed cases in the country by jurisdiction, Argentina, April-July 2009, 332 A13-8 Confirmed and under study of influenza and pandemic influenza (H1N1) 2009 by date of onset of symptoms (n = 15,455), Argentina, April-September 2009, 333 A13-9 Distribution of respiratory viruses by epidemiological week, Argentina 2009, 334 A13-10 Distribution of respiratory viruses by age group, Argentina 2009, 335 A13-11 Distribution of SARI by age group, rates per hundred thousand inhabitants, Argentina 2009 (n = 8,872), 335 A13-12 Distribution of SARI by epidemiological week of onset of symptoms, Argentina 2009 (n = 10,397 EW37), 336 A13-13 Distribution of confirmed fatalities by age group and sex, rates per hundred thousand inhabitants, Argentina 2009 (n = 505), 337 A13-14 Number of H1N1 cases among pregnant women, 2009 by day according to date of symptom onset, Argentina 2009 (n = 243), 337 A13-15 Fatal cases by underlying conditions and age, 338 A13-16 Time between events, 339 A13-17 Signs and symptoms identified in medical records, 339 A13-18 Descriptive analysis of epidemiological data 2009-H1N1 influenza A pandemic, Health Region II, Province of Buenos Aires, Argentina, May 21 through August 30, 2009, 341 A13-19 Descriptive analysis of epidemiological data of 2009-H1N1 influenza A pandemic, Tierra del Fuego, Argentina, May 21 through August 30, 2009, 341 A14-1 Reconstruction of the sequence of reassortment events leading up to the emergence of S-OIV, 344 A14-2 Genetic relationships and timing of S-OIV for each genomic segment, 345 A14-3 Phylogenetic relationships of each gene segment (PB2, PB1, PA, HA, NP, NA, M & NS) of swine influenza A viruses indicating genetic components of the swine-origin influenza A (H1N1) virus, 354 A14-4 Phylogenetic relationships scaled to time for each gene segment (PB2, PB1, PA, HA, NP, NA, M & NS) of the swine-origin influenza A (H1N1) virus as represented in Figure A14-2 of the main text but with full virus names and GenBank accession numbers, 362

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xxii TABLES, FIGURES, AND BOXES A14-5 For each gene segment (PB2, PB1, PA, HA, NP, NA, M & NS), we plot the isolation date of each influenza sequence against the genetic distance from that sequence to the root of the phylogeny, 370 BOXES WO-1 The Influenza Life Cycle, 6 WO-2 The 1976 Swine Flu Campaign: Chronology of Major Events, 11 WO-3 Clinical and Epidemiological Overview of 2009-H1N1 Influenza A, 32 WO-4 Influenza Trends, September 2009, 34 A4-1 Possible Components of a Global Access Framework, 152 A9-1 Pneumonia—China (Guangdong): RFI, 271 A9-2 Swine Flu Day by Day, 277 A11-1 Lessons Learned from the 1976 National Influenza Immunization Program (NIIP), 303 A12-1 Brief Overview of the Origin of the 1918 Pandemic H1N1 Virus and the Classical H1N1 Swine Flu Virus, 309