VECTOR-BORNE DISEASES

Understanding the Environmental, Human Health, and Ecological Connections

Workshop Summary

Rapporteurs: Stanley M. Lemon, P. Frederick Sparling, Margaret A. Hamburg, David A. Relman, 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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VECTOR-BORNE DISEASES Understanding the Environmental, Human Health, and Ecological Connections Workshop Summary Rapporteurs: Stanley M. Lemon, P. Frederick Sparling, Margaret A. Hamburg, David A. Relman, Eileen R. Choffnes, and Alison Mack Forum on Microbial Threats Board on Global Health THE NATIONAL ACADEMIES PRESS Washington, D.C. www.nap.edu

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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: Global Emerging Infec- tions Surveillance and Response System, Walter Reed Army Institute of Research, 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 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, conclusions, or recommenda- tions 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: 978-0-309-10897-3 International Standard Book Number-10: 0-309-10897-7 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: A detailed section of a stained glass window 21” × 56” depicting the natural history of influenza viruses and zoonotic exchange in the emergence of new strains was used to design the front cover. Based on the work done at St. Jude Children’s Research Hospital supported by American Lebanese Syrian Associated Charities (ALSAC) and the National Institute of Allergy and Infectious Diseases (NIAID). Artist: Jenny Hammond, Highgreenleycleugh, Northumberland, England. Suggested citation: Institute of Medicine. 2008. Vector-borne diseases: understanding the environmental, human health, and ecological connections. 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 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 STANLEY M. LEMON (Chair), School of Medicine, University of Texas Medical Branch, Galveston MARGARET A. HAMBURG (Vice-Chair), Nuclear Threat Initiative/Global Health & Security Initiative, Washington, DC P. FREDERICK SPARLING (Vice-Chair), University of North Carolina, Chapel Hill 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 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 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 DAVID A. RELMAN, Stanford University, Palo Alto, California 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 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 SARAH BRONKO, Senior Program Assistant ALISON MACK, Science Writer KATE SKOCZDOPOLE, Senior Program Associate *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, NC 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: Larry Granger, Centers for Epidemiology and Animal Health, USDA– Animal and Plant Health Inspection Services James M. Hughes, School of Medicine and Rollins School of Public Health, Emory University Emory Program in Global Infectious Diseases and Emory Center for Global Safe Water, and Southeastern Center for Emerging Biologic Threats Lonnie J. King, Center for Zoonotic, Vectorborne, and Enteric Diseases, Centers for Disease Control and Prevention 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 Melvin Worth. ix

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x REVIEWERS Appointed by the National Research Council, he was responsible for making certain that an independent examination of this report was carried out in accor- dance 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, 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. ABOUT THE WORKSHOP Vector-borne diseases such as malaria, dengue, yellow fever, plague, trypano- somiasis, and leishmaniasis have been major causes of morbidity and mortality throughout human history. During the early to mid-20th century, the vectors for yellow fever, malaria, onchocerciasis, and other diseases were effectively controlled through a variety of intervention, prevention, and control strategies. xi

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xii PREFACE However, over the past 20 to 30 years, there has been an enormous resurgence of previously “contained” vector-borne infectious diseases for a variety of reasons as well as the global emergence, reemergence, and spread of new vector-borne diseases. In addition to these threats to human health, new and emerging plant and animal vector-borne diseases have also greatly impacted regional ecologies and economies. Bluetongue virus, a disease agent transmitted to ruminants by insect vectors, costs the U.S. cattle and sheep industry an estimated $125 million annu- ally in lost trade and in diagnostic testing. Citrus tristeza virus, spread to plants by aphids, has killed tens of millions of citrus trees in outbreaks worldwide and is currently threatening the orange crop in central California with an estimated $912 million in revenues at stake. Because of their increasing economic and public health importance, coupled with their exceptional ability to cause large outbreaks of disease, vector-borne agents will continue to present significant threats to human, animal, and plant health in the future. Domestic and international capabilities to detect, identify, and control these diseases are limited for a variety of reasons. To consider the importance of vector-borne diseases in terms of their human health, ecological, and environmental implications, the Institute of Medicine’s Forum on Microbial Threats hosted a public workshop in Ft. Collins, Colorado, on June 19 and 20, 2007. Through invited presentations and discussions, partici- pants examined factors associated with the emergence of vector-borne diseases, current domestic and international detection and control capabilities, and assessed the resource needs and opportunities for improving and coordinating surveillance, diagnosis, and response to vector-borne disease outbreaks. ACKNOWLEDGMENTS 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 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 project 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: Patrick Kelley, Alison Mack, Bronwyn Schrecker, Allison Brantley, Lara Andersen, and Heather Phillips.

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xiii PREFACE 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: National Institutes of Health, National Institute of Allergy and Infectious Diseases, Centers for Disease Control and Preven- tion, and Food and Drug Administration; U.S. Department of Defense: Global Emerging Infections Surveillance and Response System, Walter Reed Army Institute of Research, 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 Laboratory; American Society for Microbiology; Sanofi Pasteur; Burroughs Wellcome Fund; Pfizer; GlaxoSmithKline; Infectious Diseases Society of America; and the Merck Com- pany 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. Stanley M. Lemon, Chair P. Frederick Sparling, Vice-Chair Margaret A. Hamburg, Vice-Chair Forum on Microbial Threats

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Contents Summary and Assessment 1 1 Vector-Borne Disease Emergence and Resurgence 41 Overview, 41 The Global Threat of Emergent/Reemergent Vector-Borne Diseases, 43 Duane J. Gubler, Sc.D. Why We Do Not Understand the Ecological Connections Between the Environment and Human Health: The Case for Vector-Borne Disease, 65 Durland Fish, Ph.D. Ecology of Emerging Vector-Borne Plant Diseases, 70 Rodrigo P. P. Almeida, Ph.D. Ecology of Disease: The Intersection of Human and Animal Health, 78 Kenneth J. Linthicum, Ph.D., Seth C. Britch, Ph.D., Assaf Anyamba, Ph.D., Jennifer Small, Compton J. Tucker, Ph.D., Jean-Paul Chretien, M.D., Ph.D., and Ratana Sithiprasasna, Ph.D. Climate Change and Health: Global to Local Influences on Disease Risk, 88 Jonathan A. Patz, M.D., M.P.H., and Sarah H. Olson Climate Change and Vector-Borne Disease: Update on Climate Effects on Lyme Disease and West Nile Virus in North America, 104 Jonathan A. Patz, M.D., M.P.H., and Christopher K. Uejio, M.A. References, 111 xv

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xvi CONTENTS 2 Vector-Borne Disease Detection and Control 127 Overview, 127 Longitudinal Field Studies Will Guide a Paradigm Shift in Dengue Prevention, 132 Thomas W. Scott, Ph.D., and Amy C. Morrison, Ph.D. Innovative Decision Support and Vector Control Approaches to Control Dengue, 150 Lars Eisen, Ph.D., and Barry J. Beaty, Ph.D. West Nile Virus, 162 Lyle R. Petersen, M.D., M.P.H. Rift Valley Fever Is an Emerging Arthropod-Borne Virus, 173 C. J. Peters, M.D. The Implications of Entomological Monitoring and Evaluation for Arthropod Vector-Borne Disease Control Programs, 178 Michael Coleman, Ph.D., and Janet Hemingway, Ph.D. Vector-Borne Zoonotic Diseases and Their Ecological and Economic Implications: Bluetongue Disease in Europe, 190 Bennie I. Osburn, Ph.D., D.V.M. Environmental Factors Influence Transmission of Sin Nombre Hantavirus Between Rodents (and to Humans?), 200 Charles H. Calisher, Ph.D., James N. Mills, Ph.D., J. Jeffrey Root, Ph.D., Jeffrey B. Doty, M.S., Barry J. Beaty, Ph.D. References, 217 3 Integrating Strategies to Address Vector-Borne Disease 241 Overview, 241 Needs and Opportunities to Control Vector-Borne Diseases: Responses to the IOM Microbial Threats to Health Committee Recommendations, 243 Barry J. Beaty, Ph.D., and Lars Eisen, Ph.D. Integration of Strategies: Surveillance, Diagnosis, and Response, 263 Roger S. Nasci, Ph.D. Surveillance, Diagnosis, and Response: Integration of Strategies, 268 Sherrilyn Wainwright, D.V.M., M.P.H. Confronting Vector-Borne Diseases in an Age of Ecologic Change, 274 David M. Morens, M.D. The Vector Biology Program at the National Institute of Allergy and Infectious Diseases, 284 Adriana Costero, Ph.D. References, 287

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xvii CONTENTS Appendixes A Agenda 297 B Acronyms 301 C Forum Member Biographies 305

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Tables, Figures, and Boxes TABLES SA-1 Estimates of the Global Burden of Disease Caused by Major Vector- Borne Diseases, 6 SA-2 Studies Suggesting Links Between ENSO-Driven Variations in Temperature and Precipitation and Arthropod-Borne Infectious Diseases, 20 1-1 Emergent/Reemergent Arboviral Diseases of Humans, 48 1-2 Exotic Infectious Diseases That Have Recently Been Introduced to the United States, 62 1-3 Principal Epidemic Vector-Borne Diseases Affecting Humans at the Beginning of the 21st Century, 63 1-4 Pathogens of Tomorrow: From Whence They Will Come?, 64 1-5 Temperature Thresholds of Some Human Pathogens and Their Vectors, 95 2-1 Reported West Nile Virus Disease Cases in Humans, by Clinical Syndrome, United States, 1999-2006, 165 2-2 Viral Proteins and Functions, 192 2-3 Location of Culicoides Vectors for Bluetongue Virus, 193 2-4 Recognized Hantaviruses (to April 2007), 202 2-5 Recaptured Deer Mice (Peromyscus maniculatus), by Sex and Maximum Number of Weeks Between First and Last Capture, Pinyon Canyon Maneuver Site, Southeastern Colorado, January 1995- November 2000, 208 xviii

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xix TABLES, FIGURES, AND BOXES 2-6 Incidence of IgG Antibody Reactive with Sin Nombre Virus in Deer Mice (Peromyscus maniculatus) Recaptured and Sampled at Least Twice at Pinyon Canyon Maneuver Site, Southeastern Colorado, January 1995-November 2000, 208 3-1 Factors in Emergence of Infectious Diseases, 246 3-2 Factors Conditioning the Resurgence and Emergence of Vector-Borne Diseases, 247 3-3 Innovative Approaches to Restoring Human Resource Capacity in Vector-Borne Diseases, 253 FIGURES SA-1 Deaths from vector-borne diseases, 5 SA-2 Dengue/dengue hemorrhagic fever, average annual number of cases reported to WHO, 1955-2005, 7 SA-3 The epidemiological triad, 12 SA-4 Factors affecting plant disease outbreaks, 13 SA-5 The epidemiological effects of urbanization and environmental change, 16 SA-6 Map of the distribution of bluetongue throughout Europe as of November 28, 2007, 23 1-1 Reported Lyme disease cases by year, United States, 1982-2005, 46 1-2 Suspected spread of pneumonic plague from India, 1994, 47 1-3 The sequential westward movement of West Nile virus in the United States by year, 50 1-4 Epidemic West Nile virus in the United States, 1999-2006, 51 1-5 Migratory bird flyways in the western hemisphere, 52 1-6 Epidemics caused by West Nile virus, 1937-2007, 53 1-7 Phylogenetic tree of West Nile viruses based on sequence of the envelope gene, 54 1-8 Distribution of Aedes aegypti in American countries in 1930, 1970, and 2007, 56 1-9 Countries reporting confirmed DHF prior to 1981 and 1981 to 2007, 56 1-10 Mean annual global reported cases of DEN/DHF to the World Health Organization, by decade, 1955-2005, 57 1-11 The global distribution of dengue virus serotypes, (A) 1970 and (B) 2007, 61 1-12 Model illustrating a hypothesis on how newly introduced vectors may drive new disease epidemics, 77 1-13 Dengue incidence calculated per 100,000 population for Thailand from 1973 to 1999 plotted against OLR anomalies from 1979 to 2000, 81

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xx TABLES, FIGURES, AND BOXES 1-14 NDVI (dashed line) and rainfall anomalies (bars) for Lamu, Kenya, between 1998 and 2006, 82 1-15 Southern Oscillation Index (SOI) anomalies between January 1950 and 2006, 82 1-16 Diama Dam on Senegal River (left), and resulting flooding (center) and vegetation development (right) in Mauritania in January 1988 after the closure of dam, 83 1-17 SST anomalies for October 2006 (top) and OLR anomalies for October 2006 (bottom), 85 1-18 Shipping lanes entering eastern U.S. ports and inland container facilities from offshore destinations, 87 1-19 Variations in the mean surface temperatures recorded (using thermometers) across the planet in the past 140 years (a) and (using a combination of tree-ring, coral, and ice-core analysis and, for recent decades, thermometers) in the northern hemisphere over the past 10,000 years (b), 89 1-20 The increasing trend in strong tropical storms seen over the last 50 years, 91 1-21 The potential impact of sea-level rise on Bangladesh, 92 1-22 As this graph produced by McDonald (1957) illustrates, air temperature has a marked effect on the extrinsic incubation periods (EIPs—the times taken by the parasites to produce sporozoites in their mosquito vectors) of Plasmodium falciparum and P. vivax, 97 1-23 Areas of the African highlands that, though currently nonendemic, are probably vulnerable to malaria as the result of climate warming ( ), 98 1-24 Comparison of the maximum (o), mean (®), and minimum (∆) temperatures recorded within huts in deforested agricultural lands with the corresponding maximum (•), mean (ß), and minimum (▲) temperatures recorded within huts in forests, 99 1-25 Correlation between simulated, climate-driven variations in Aedes aegypti mosquito density (o) and observed variations in the annual numbers of cases (•) of dengue, including dengue haemorrhagic fever, in three countries, 101 1-26 The World Health Organization’s estimates of mortality attributable to climate change by the year 2000, 103 1-27 Decrease in the time before an infectious mosquito can retransmit a virus or extrinsic incubation period from laboratory experiments, 109 1-28 (A) Long-term climatological average summer (June-September) temperatures for the United States and (B-D) anomalies for each summer from 2002 to 2004, 110 2-1 Flow scheme for a Dengue Decision Support System, 154

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xxi TABLES, FIGURES, AND BOXES 2-2 Example from Chetumal, Mexico, of quality of imagery accessed through Google Earth, 155 2-3 Outline of data potentially included in a full-capacity Dengue Decision Support System, 157 2-4 Phylogenetic tree of West Nile virus, 163 2-5 Equine and human West Nile virus neuroinvasive disease cases, by year, United States, 164 2-6 West Nile virus activity and human neuroinvasive disease incidence per million population, by county, United States, 1999-2006, 166 2-7 Reported number of human West Nile virus disease cases, by week of symptom onset, 2006, United States, 167 2-8 Human cases of West Nile virus and St. Louis encephalitis neuroinvasive disease, by year, 1932-2006, United States, 168 2-9 Phylogenetic analysis of West Nile virus E gene sequences, by (A) year and (B) location, United States, 172 2-10 By monitoring the species density on Bioko Island, Equatorial Guinea, the malaria control program was able to detect a reduced impact of IRS with pyrethroid on An. gambiae compared to An. funestus, 180 2-11 Resistance in Africa, 1950-2006, 182 2-12 Insecticide resistance monitoring methods, 183 2-13 Monitoring of insecticide resistance in Mozambique has resulted in several policy changes on the insecticide of choice for the country’s IRS program, 185 2-14 Insecticide rotation, 186 2-15 Malaria Decision Support System, 188 2-16 Distribution of Culicoides episystems and bluetongue virus topotypes, 194 2-17 Bluetongue virus and Culicoides vector cycle, 196 2-18 Progression of bluetongue viruses emergence in Europe, 198 2-19 Overview of Red Rocks Canyon, Pinon Canyon Maneuver Site, southeastern Colorado, 206 2-20 Close-up view of rocky area in Red Rocks Canyon, Pinon Canyon Maneuver Site, southeastern Colorado, 206 2-21 Quarterly precipitation as recorded at three weather stations in or near the Pinon Canyon Maneuver Site, southeastern Colorado, 1995- 2000, 210 2-22 Deviations from the 50-year mean (1951-2000) for quarterly (A) mean maximum and (B) mean minimum temperatures and quarterly precipitation at Rocky Ford, Colorado, weather station, 211 2-23 (A) Quarterly trap success for deer mice and total quarterly precipitation; (B) percent of adults in reproductive condition and percent of captures consisting of juveniles, at two mark-recapture sites in southeastern Colorado, 1995-2000, 212

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xxii TABLES, FIGURES, AND BOXES 2-24 The 1991-1993 El Niño and some of its consequences in the southwestern United States, 215 2-25 The 1997-1998 El Niño and some of its consequences in the southwestern United States, 216 3-1 Available funding mechanisms for research, 286 BOxES 1-1 Some Effects of Weather and Climate on Vector- and Rodent-Borne Diseases, 106 2-1 Key Questions for Development of Innovative, Sustainable, and Cost- Effective Dengue Prevention, 144