GLOBAL CLIMATE CHANGE AND EXTREME WEATHER EVENTS

Understanding the Contributions to Infectious Disease Emergence

WORKSHOP SUMMARY

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

Forum on Microbial Threats

Board on Global Health

INSTITUTE OF MEDICINE OF THE NATIONAL ACADEMIES

THE NATIONAL ACADEMIES PRESS

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Global Climate ChanGe and extreme Weather events Understanding the Contributions to infectious disease emergence Workshop sUmmary Rapporteurs: David A. Relman, Margaret A. Hamburg, Eileen R. Choffnes, and Alison Mack 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 Develop- ment; Lawrence Livermore National Laboratory; American Society for Microbiology; Sanofi Pasteur; Burroughs Wellcome Fund; Pfizer; GlaxoSmithKline; Infectious Diseases Society of America; and the Merck Company Foundation. Any opinions, findings, conclu- sions, 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: 978-0-309-12402-7 International Standard Book Number-10: 0-309-12402-6 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 2008 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: The cover image is a global anomaly mosaic of the combined normalized differ- ence vegetation index (depicted over land surfaces) and sea surface temperatures (depicted over oceans) for January 2007 during the peak period of the 2006-2007 El Niño/Southern Oscillation warm event. SOURCE: Data processing and analysis: Jennifer Small, Edwin Pak, Assaf Anyamba, Compton J. Tucker, GIMMS Group, NASA Goddard Space Flight Center. This image was provided by Dr. Assaf Anyamba of the University of Maryland Baltimore County and NASA Goddard Space Flight Center, GIMMS Group. Suggested citation: IOM (Institute of Medicine). 2008. Global climate change and extreme weather events: understanding the contributions to infectious disease emergence. Wash- ington, 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 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 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 THREATS DAVID A. RELMAN (Chair), Stanford University, Palo Alto, California MARGARET A. HAMBURG (Vice Chair), Nuclear Threat Initiative/Global Health & Security Initiative, Washington, DC DAVID W. K. ACHESON, Center for Food Safety and Applied Nutrition, Food and Drug Administration, Rockville, Maryland RUTH L. BERKELMAN, Emory University, Center for Public Health Preparedness and Research, Rollins School of Public Health, Atlanta, Georgia ENRIQUETA C. BOND, Burroughs Wellcome Fund, Research Triangle Park, North Carolina ROGER G. BREEZE, Centaur Science Group, Washington, DC STEVEN J. BRICKNER, Pfizer Global Research and Development, Pfizer Inc., Groton, Connecticut GAIL H. CASSELL, Eli Lilly & Company, Indianapolis, Indiana BILL COLSTON, Lawrence Livermore National Laboratory, Livermore, California RALPH L. ERICKSON, Global Emerging Infections Surveillance and Response System, Department of Defense, Silver Spring, Maryland MARK B. FEINBERG, Merck Vaccine Division, Merck & Co., West Point, Pennsylvania J. PATRICK FITCH, National Biodefense Analysis and Countermeasures Center, Frederick, Maryland 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, Division of Microbiology and Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland DAVID L. HEYMANN, Polio Eradication, World Health Organization, Geneva, Switzerland PHIL HOSBACH, New Products and Immunization Policy, Sanofi Pasteur, Swiftwater, Pennsylvania IOM Forums and Roundtables do not issue, review, or approve individual documents. The responsibil- ity for the published workshop summary rests with the workshop rapporteur(s) and the institution. v

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JAMES M. HUGHES, Global Infectious Diseases Program, Emory University, Atlanta, Georgia STEPHEN A. JOHNSTON, Arizona BioDesign Institute, Arizona State University, Tempe GERALD T. KEUSCH, Boston University School of Medicine and Boston University School of Public Health, Massachusetts RIMA F. KHABBAZ, National Center for Preparedness, Detection and Control of Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia LONNIE J. KING, Center for Zoonotic, Vectorborne, and Enteric Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia GEORGE W. KORCH, U.S. Army Medical Research Institute for Infectious Diseases, Fort Detrick, Maryland JOSHUA LEDERBERG,* The Rockefeller University, New York STANLEY M. LEMON, School of Medicine, University of Texas Medical Branch, Galveston LYNN G. MARKS, Medicine Development Center, GlaxoSmithKline, Collegeville, Pennsylvania EDWARD MCSWEEGAN, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 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, Arizona BioDesign Institute, Arizona State University, Tempe GARY A. ROSELLE, Central Office, Veterans Health Administration, Department of Veterans Affairs, Washington, DC JANET SHOEMAKER, Office of Public Affairs, American Society for Microbiology, Washington, DC P. FREDERICK SPARLING, University of North Carolina, Chapel Hill BRIAN J. STASKAWICZ, Department of Plant and Microbial Biology, University of California, Berkeley 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 SARAH BRONKO, Senior Program Assistant ALISON MACK, Science Writer *Deceased February 2, 2008. vi

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BOARD ON GLOBAL HEALTH Margaret Hamburg (Chair), Consultant, Nuclear Threat Initiative, Washington, DC George Alleyne, Director Emeritus, Pan American Health Organization, Washington, DC Donald Berwick, Clinical Professor of Pediatrics and Health Care Policy, Harvard Medical School, and President and Chief Executive Officer, Institute of Healthcare Improvement, Boston, Massachusetts Jo Ivey Boufford (IOM Foreign Secretary), President, New York Academy of Medicine, New York David R. Challoner, Vice President for Health Affairs, Emeritus, University of Florida, Gainesville Ciro de Quadros, Albert B. Sabin Vaccine Institute, Washington, DC 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 Richard Guerrant, Thomas H. Hunter Professor of International Medicine and Director, Center for Global Health, University of Virginia School of Medicine, Charlottesville 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 Jeffrey Koplan, Vice President for Academic Health Affairs, Emory University, Atlanta, Georgia Sheila Leatherman, Research Professor, University of North Carolina School of Public Health, Chapel Hill Michael Merson, Director, Duke Global Health Institute, Duke University, Durham, North Carolina Mark L. Rosenberg, Executive Director, Task Force for Child Survival and Development, Emory University, Decatur, Georgia Philip Russell, Professor Emeritus, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland Staff Patrick Kelley, Director Allison Brantley, Senior Program Assistant 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 deliberative process. We wish to thank the following individuals for their review of this report: Ralph L. Erickson, DoD-Global Emerging Infections Surveillance and Response System, Walter Reed Army Institute of Research Jonathan Patz, Center for Sustainability and the Global Environment, University of Wisconsin-Madison Jeffrey Shaman, College of Oceanic and Atmospheric Sciences, Oregon State University Mark Wilson, Department of Epidemiology, The University of Michigan 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 ix

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x REVIEWERS 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.

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Preface 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, to identify areas in need of greater atten- tion, to clarify policy issues by enhancing knowledge and identifying points of agreement, and to 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. ABOUT THE WORKSHOP Long before the “germ theory” of disease was described, late in the nine- teenth century,1 humans have known that climatic conditions influence the appear- 1 Pasteur, L. 1878. Germ theory and its applications to medicine and surgery. Read before the French Academy of Sciences, April 29, 1878. Published in Comptes rendus de l’Academie des Sci- ences, lxxxvi, pp. 1037-1043. Taken from Scientific papers (physiology, medicine, surgery, geology). New York: P. F. Collier and Son [c1910]. The Harvard classics v. 38. Modern History Sourcebook; http://www.fordham.edu/halsall/mod/1878pasteur-germ.html (accessed October 31, 2007). xi

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xii PREFACE ance and spread of epidemic diseases. As was pointed out in the report Under the Weather: Climate, Ecosystems, and Infectious Disease, “Since the dawn of medical science, people have recognized connections between a change in the weather and the appearance of epidemic disease. Roman aristocrats retreated to hill resorts each summer to avoid malaria. South Asians learned early that, in high summer, strongly curried foods were less likely to cause diarrhea.” 2 Ancient notions about the effects of weather and climate on disease remain in the medical and colloquial lexicon, in terms such as “cold” for rhinovirus infec- tions; “malaria,” derived from the Latin for “bad air”; and the common complaint of feeling “under the weather.” Today, the evidence is mounting that Earth’s climate is changing,3 leading researchers to view the long-standing relationships between climate and disease from a global perspective. Variations in climate may affect the health of humans, animals, and plants through direct impacts such as extreme heat or cold, or indirectly, by changing environments—in ways that may, for example, alter the geographic distribu- tion or transmission dynamics of infectious diseases. The most recent report of the IPCC’s Working Group II, whose members studied the influence of climate change on biological and social systems, stated with “very high confidence” that “climate change currently contributes to the global burden of disease and prema- ture deaths.” However, “at this early stage the effects are small but are projected to progressively increase in all countries and regions.”4 The warming of the Earth is already contributing to the worldwide burden of disease and premature deaths, and is anticipated to influence the transmission dynamics and geographic distribution of malaria, dengue, tick-borne diseases, cholera, and other diarrheal diseases.5 In the specific case of the relationship between climate and infectious diseases, it is important to recognize that a com- plex “web of causation” determines the distribution and transmission of infec- tious disease agents.6 In addition to climate, factors influencing the geographic distribution and transmission of disease agents include: land-use patterns; a variety of social, demographic, and geographical variables; trade and transporta- tion; human and animal migration; and public health interventions. Some of these factors are closely interrelated and influenced—directly or indirectly—by local, regional, or global variations in climate. 2 NRC (National Research Council). 2001. Under the weather: climate, ecosystems, and infectious disease. Washington, DC: National Academy Press. 3 IPCC (Intergovernmental Panel on Climate Change). 2007a. Climate change 2007: the physical science basis. Working Group I contribution to the Fourth Assessment Report of the IPCC. Cam- bridge, UK: Cambridge University Press. 4 IPCC. 2007b. Climate change 2007: climate change impacts, adaptation, and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the IPCC. Cambridge, UK: Cambridge University Press. 5 IPCC (2007b). 6 NRC (2001).

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xiii PREFACE The heating of the planet is also accelerating the hydrological cycle, increas- ing the likelihood of extreme weather events such as droughts, heavy precipi- tation, heat waves, hurricanes, typhoons, and cyclones. The projected health impacts of climate change and extreme weather events are predominately nega- tive, with the most severe impacts in low-income countries where the capacity to adapt is weakest. Developed countries are also vulnerable to the health effects of extreme temperatures, as was demonstrated in 2003 when tens of thousands of Europeans died as a result of record-setting summer heat waves.7 Climate change is expected to converge with, and intensify, additional contributors to infectious disease emergence and reemergence including global trade and transportation, land use, and human migration.8 The Forum on Microbial Threats hosted a public workshop in Washington, DC, on December 4 and 5, 2007, to consider the possible infectious disease impacts of global climate change and extreme weather events on human, animal, and plant health, as well as their implications for global and national security. Through invited presentations and discussions, participants explored a range of topics related to climate change and infectious diseases, including the ecological and environmental contexts of climate and infectious diseases; direct and indirect influences of extreme weather events and climate change on infectious diseases; environmental trends and their influence on the emergence, reemergence, and movement of vector- and non-vector-borne infectious diseases; opportunities and challenges for the surveillance, prediction, and early detection of climate-related outbreaks of infectious diseases; and the international policy implications of the potentially far-reaching health impacts of climate change. ACKNOWLEDGMENTS The Forum on Microbial Threats and the IOM wish to express their warmest appreciation to the individuals and organizations that gave their valuable time to provide information and advice to the Forum through their participation in this workshop. A full list of presenters can 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 Eileen Choffnes, director of the Forum, Kate Skoczdopole, senior program associate, and Sarah Bronko, 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 translating the workshop’s proceedings and 7 Kovats, R. S., and A. Haines. 2005. Global climate change and health: recent findings and future steps. Canadian Medical Association Journal 172(4):501-502. 8 IOM (Institute of Medicine). 2003. Microbial threats to health: emergence, detection, and re- sponse. Washington, DC: The National Academies Press.

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xiv PREFACE discussion into this workshop summary. We would also like to thank Dr. Assaf Anyamba of the NASA Goddard Space Flight Center and the University of Maryland Baltimore County for his invaluable contributions to this volume. Special thanks to the following IOM staff and consultants for their valuable contributions to this activity: Alison Mack, Bronwyn Schrecker, Lara Andersen, and Florence Poillon. 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; Lawrence Livermore National Labora- tory; 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 neces- sarily those of the Forum on Microbial Threats or its sponsors. David A. Relman, Chair Margaret A. Hamburg, Vice Chair Forum on Microbial Threats

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Contents Summary and Assessment 1 1 Climate Change Challenges 54 Overview, 54 Climate Change, Extreme Events, and Human Health, 57 Andy Haines, M.B.B.S., M.D. Climate Change and Human Health, 74 Paul R. Epstein, M.D., M.P.H. Climate Change Futures: Health, Ecological, and Economic Dimensions, 79 The Center for Health and the Global Environment, Harvard Medical School Impacts of Global Climate Change on Infectious Diseases, 90 Donald S. Burke, M.D. References, 99 2 Climate, Ecology, and Infectious Disease 104 Overview, 104 The Marine Environment and Human Health: The Cholera Model, 109 Rita Colwell, Ph.D. Extreme Weather and Epidemics: Rift Valley Fever and Chikungunya Fever, 116 Jean-Paul Chretien, M.D., Ph.D.; Assaf Anyamba, Ph.D.; Jennifer Small, M.A.; Compton J. Tucker, Ph.D.; Seth C. Britch, Ph.D.; and Kenneth J. Linthicum, Ph.D. xv

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xvi CONTENTS Plague and Climate, 128 Nils Chr. Stenseth, Dr.philos. Climate Change and Plant Disease Risk, 143 Karen A. Garrett, Ph.D. Climate Change and Infectious Disease: Impact on Human Populations in the Arctic, 155 Alan J. Parkinson, Ph.D. References, 168 3 Historical, Scientific, and Technological Approaches to Studying the Climate-Disease Connection 179 Overview, 179 Drought, Epidemic Disease, and Massive Population Loss: 1,000 Years of Record in Mexico, 183 Rodolfo Acuña-Soto, M.D., M.Sc., D.Sc.; David W. Stahle, Ph.D.; Matthew D. Therrell, Ph.D.; and José Villanueva Diaz, Ph.D. Wildlife Health as an Indicator of Climate Change, 192 Pablo M. Beldomenico, M.V., M.P.V.M., Ph.D.; Damien O. Joly, Ph.D.; Marcela M. Uhart, M.V.; and William B. Karesh, D.V.M. Use of Climate Variation in Vector-Borne Disease Decision Support Systems, 198 William K. Reisen, Ph.D., and Christopher M. Barker, M.S. References, 212 4 Policy Implications of the Health Effects of Climate Change and Extreme Weather Events 219 Overview, 219 Influences of Migration and Population Mobility, 222 Douglas W. MacPherson, M.D., M.Sc. (CTM), F.R.C.P.C., and Brian D. Gushulak, M.D. Climate Change, Infectious Disease, and International Public Health Policy, 230 Diarmid Campbell-Lendrum, D.Phil. References, 238 Appendixes A Agenda 245 B Acronyms 250 C Glossary 253 D Forum Member Biographies 258

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Tables, Figures, and Boxes TABLES SA-1 Observed Changes in North American Extreme Events, Assessment of Human Influence for the Observed Changes, and Likelihood That the Changes Will Continue Through the Twenty-first Century, 7 SA-2 Examples of Diseases Influenced by Environmental Conditions, 12 1-1 Examples of Environmental Factors Known to Be Strongly Associated with Certain Specific Infectious Diseases, 92 2-1 Cholera Cases Officially Reported to WHO, 2004—Selected Countries, 110 2-2 Factors in Emergence and Spread of Rift Valley Fever and Chikungunya Fever, 126 3-1 Famines in the Valley of Mexico, 185 3-2 Major Epidemics in the Valley of Mexico, 186 3-3 Deadliest Epidemics in Central Mexico, 187 3-4 Epidemics of Hemorrhagic Fevers in the Valley of Mexico, 190 3-5 California Mosquito-Borne Virus Surveillance and Response Plan Model Scores for Each Surveillance Parameter, 206 4-1 Mobile Population Characteristics and Estimated Annual Magnitudes, 223 xvii

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xviii TABLES, FIGURES, AND BOXES FIGURES SA-1 People affected by hydrometeorological disaster (millions per year), 8 SA-2 Potential health effects of climate variability and change, 11 SA-3 The epidemiological triad, 13 SA-4 The Convergence Model, 14 SA-5 Progression of bluetongue viruses emergence in Europe, 16 SA-6 Hot spots of potential elevated risk for disease outbreaks under El Niño conditions, 2006-2007, 17 SA-7 (A) Using satellites to track Rift Valley fever; (B) January 2007 combined global Normalized Difference Vegetation Index (NDVI) (depicted over land surfaces) and sea surface temperature (SST) (depicted over oceans) anomaly mosaic, 19 SA-8 Interconnectedness of terrestrial, aquatic, and marine food webs, 25 SA-9 Ranavirus-associated disease in frogs, 26 SA-10 Viral hemorrhagic septicemia (VHS) Rhabdoviridae novirhabdovirus, 26 SA-11 Chytridiomycosis (Batrachochytrium dendrobatidis) in Chiricahua leopard frog (New Mexico), 27 SA-12 Perkinsus—wood frog (Rana sylvatica) tadpole with massively enlarged yellow liver, 27 SA-13 The Arctic ice cap, September 2001 (Top) and September 2007 (Bottom), 29 SA-14 Arctic shipping shortcuts, 31 SA-15 Global distribution of relative risk of an emerging infectious disease (EID) event, 37 SA-16 Variation in Earth’s average surface temperature over the past 20,000 years, 44 SA-17 The Arctic is experiencing the fastest rate of warming as its reflective covering of ice and snow shrinks, 45 SA-18 Observed changes in (A) global average surface temperature; (B) global average sea level rise from tide gauge (blue) and satellite (red) data; and (C) Northern Hemisphere snow cover for March-April, 46 SA-19 Drought is seizing more territory in the wake of mounting temperatures, 47 1-1 Observed changes in (A) global average surface temperature; (B) global average sea level rise from tide gauge (blue) and satellite (red) data; and (C) Northern Hemisphere snow cover for March-April, 59 1-2 Multimodel averages and assessed ranges for surface warming (compared to the 1980-1999 base period) for the SRES scenarios A2 (red), A1B (green), and B1 (blue), shown as continuations of the twentieth-century simulation, 60

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xix TABLES, FIGURES, AND BOXES 1-3 Pathways by which climate change may affect human health, including infectious diseases, 63 1-4 ENSO teleconnections and risk map for malaria, 65 1-5 Relative vulnerability of coastal deltas as indicated by estimates of the population potentially displaced by current sea-level trends to 2050 (extreme >1 million; high 1 million to 50,000; medium 50,000 to 5,000), 68 1-6 Potential health effects of drought in developing countries, 68 1-7 Hurricane Katrina passing over the Gulf of Mexico, 75 1-8 Increase from 1992 (left) to 2002 (right) in the amount of the Greenland ice sheet melted in the summer, 78 1-9 Warm ocean waters fuel hurricanes, 81 1-10 These data are taken from EMDAT (Emergency Events Database) from 1975 to 2002, 84 1-11 Transmission of influenza from infected guinea pigs to uninfected exposed guinea pigs under different experimental conditions in which ambient temperature and relative humidity were varied, 94 1-12 Graph showing the amplitude of oscillations (y axis, peak-trough ratio) as a function of the endogenous oscillation period (x axis) in a stochastic forced S-I-R-S epidemic model for 2,000 sets of randomly chosen parameters, 96 1-13 Influenza virus types isolated in the United States between 1997 and 2007, 97 1-14 Multiyear time series of incidence of dengue hemorrhagic fever cases in Bangkok decomposed using the Empirical Mode Decomposition method into three modes of different approximate frequencies, 98 2-1 Bangladesh border, barrier islands, and location of Dacca, Matlab, Mathbaria, and Bakerganj, 111 2-2 Environmental parameters (top) and predicted versus actual cholera incidence rate (bottom), 115 2-3 Global SST anomalies, September 2006, 119 2-4 Seasonal rainfall anomalies in the Horn of Africa, September- November 2006, 120 2-5 NDVI anomalies (A) and RVF calculated risk (B) in the Horn of Africa, December 2006, 121 2-6 USAMRU-K mosquito collection sites (blue dots) and RVF risk assessment, December 2006, 122 2-7 Cumulative monthly rainfall (dotted line) and long-term mean cumulative monthly rainfall (solid line) in Lamu and Mombasa, 124 2-8 Outgoing longwave radiation (OLR) anomalies, July 2007, for the Mediterranean region, 125

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xx TABLES, FIGURES, AND BOXES 2-9 The Convergence Model, 127 , 2-10 The global distribution of plague, 129 2-11 The global distribution of plague: (A) cumulative number of countries that reported plague to WHO per continent, from 1954-1998; (B) the temporal distribution of plague cases by continent, from 1954-1998, also from WHO, 130 2-12 Routes followed by the three plague pandemic waves (labeled 1, 2, and 3), 131 2-13 Possible transmission pathways for the plague bacterium, Yersinia pestis, 133 2-14 The field data used in Stenseth et al. (2006) were collected in a natural plague focus in Kazakhstan, 135 2-15 Relationship between the likelihood of detecting plague (solid line) in gerbils and past burrow occupancy rates together with data on presence or absence of plague at two sites, 137 2-16 Tree-ring data suggesting that conditions during the Black Death and the Third Pandemic were similar, 139 2-17 The modified trophic cascade model of Parmenter et al. (1999), 141 2-18 Estimated potato late blight severity in the Altiplano area of Peru and Bolivia based on weather measures during 2001-2004 used in a late blight forecasting model, 147 2-19 The plant disease triangle, illustrating the relationship between host, pathogen, and environment necessary for disease to occur, 151 2-20 The circumpolar region showing administrative jurisdictions, 157 2-21 The circumpolar region showing indigenous and nonindigenous population distributions, 158 2-22 The Arctic ice cap, September 2001 (Top) and September 2007 (Bottom), 159 2-23 Proposed northwest and northeast shipping lanes through the Arctic Ocean joining the Atlantic and Pacific Oceans, 160 3-1 Sequence of surveillance data collected during seasonal virus amplification, 182 3-2 West Nile virus transmission cycle, 199 3-3 TOPS system brings ground and remote measures of climate into ecological models to monitor and forecast risk, 201 3-4 Incidence of human West Nile virus cases per million population and temperature anomalies for the United States, 2003-2007, 203 3-5 Sequence of surveillance data collected during seasonal virus amplification, 205 Data flow through the Surveillance Gateway© system, 205 3-6 3-7 California mosquito district risk levels 1-5 for WNV transmission, 208

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xxi TABLES, FIGURES, AND BOXES 3-8 Intervention options for WNV shown in relation to (A) the amplification curve and (B) the transmission cycle, 210 4-1 Number of publications in PubMed referring to “health” and either “climate change” or “global warming” from 1990 to 2007, 234 BOxES SA-1 Under the Weather Key Findings: Linkages Between Climate and Infectious Diseases, 4 SA-2 Emerging Infectious Diseases in the Aquatic-Marine Continuum, 26 SA-3 Under the Weather Recommendations for Future Research and Surveillance, 43 1-1 Regional-Scale Changes, 61 1-2 Key Points, 85 1-3 Vulnerabilities in the Energy Sector, 86 1-4 Case Studies in Brief, 88 4-1 The International Mandate for Stronger Action on Health and Climate Change, 235

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