Vector-Borne Diseases: Understanding the Environmental, Human Health, and Ecological Connections, Workshop Summary (Forum on Microbial Threats)

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

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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 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 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: International Standard Book Number-10:

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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" x 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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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 Biologies 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

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

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.

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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, evidence, 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, USDAAnimal 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 comments 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.

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REVIEWERS

Appointed by the National Research Council, 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.

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 agreement, and inform decision makers about science and policy issues. The Forum seeks to illuminate issues rather than resolve them; for this reason, it does not provide advice or recommendations on any specific policy initiative pending before any agency or organization. Its value derives instead from the diversity of its membership and from the contributions that individual members make throughout the activities of the Forum. In 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, trypanosomiasis, 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.

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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 annually 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, participants 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 discussion 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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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 Prevention, 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 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. Stanley M. Lemon, Chair P. Frederick Sparling, Vice-Chair Margaret A. Hamburg, Vice-Chair Forum on Microbial Threats

Contents

Summary and Assessment 1

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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

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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 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

CONTENTS

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Appendixes A B C

Agenda Acronyms Forum Member Biographies

297 301 305

Tables, Figures, and Boxes

TABLES SA-1 Estimates of the Global Burden of Disease Caused by Major VectorBorne Diseases, 6 SA-2 Studies Suggesting Links Between ENSO-Driven Variations in Temperature and Precipitation and Arthropod-Borne Infectious Diseases, 20 1-1 1-2 1-3 1-4 1-5

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Emergent/Reemergent Arboviral Diseases of Humans, 48 Exotic Infectious Diseases That Have Recently Been Introduced to the United States, 62 Principal Epidemic Vector-Borne Diseases Affecting Humans at the Beginning of the 21st Century, 63 Pathogens of Tomorrow: From Whence They Will Come?, 64 Temperature Thresholds of Some Human Pathogens and Their Vectors, 95 Reported West Nile Virus Disease Cases in Humans, by Clinical Syndrome, United States, 1999-2006, 165 Viral Proteins and Functions, 192 Location of Culicoides Vectors for Bluetongue Virus, 193 Recognized Hantaviruses (to April 2007), 202 Recaptured Deer Mice {Peromyscus maniculatus), by Sex and Maximum Number of Weeks Between First and Last Capture, Pinyon Canyon Maneuver Site, Southeastern Colorado, January 1995November 2000, 208 xv u i

TABLES, FIGURES, AND BOXES

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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

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Factors in Emergence of Infectious Diseases, 246 Factors Conditioning the Resurgence and Emergence of Vector-Borne Diseases, 247 Innovative Approaches to Restoring Human Resource Capacity in Vector-Borne Diseases, 253

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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 S A-6 Map of the distribution of bluetongue throughout Europe as of November 28, 2007, 23 1-1 1-2 1-3 1-4 1-5 1-6 1-7 1-8 1-9 1-10 1-11 1-12 1-13

Reported Lyme disease cases by year, United States, 1982-2005, 46 Suspected spread of pneumonic plague from India, 1994, 47 The sequential westward movement of West Nile virus in the United States by year, 50 Epidemic West Nile virus in the United States, 1999-2006, 51 Migratory bird fly ways in the western hemisphere, 52 Epidemics caused by West Nile virus, 1937-2007, 53 Phylogenetic tree of West Nile viruses based on sequence of the envelope gene, 54 Distribution of Aedes aegypti in American countries in 1930, 1970, and 2007, 56 Countries reporting confirmed DHF prior to 1981 and 1981 to 2007, 56 Mean annual global reported cases of DEN/DHF to the World Health Organization, by decade, 1955-2005, 57 The global distribution of dengue virus serotypes, (A) 1970 and (B) 2007, 61 Model illustrating a hypothesis on how newly introduced vectors may drive new disease epidemics, 77 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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NDVI (dashed line) and rainfall anomalies (bars) for Lamu, Kenya, between 1998 and 2006, 82 Southern Oscillation Index (SOI) anomalies between January 1950 and 2006, 82 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 SST anomalies for October 2006 (top) and OLR anomalies for October 2006 (bottom), 85 Shipping lanes entering eastern U.S. ports and inland container facilities from offshore destinations, 87 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 The increasing trend in strong tropical storms seen over the last 50 years, 91 The potential impact of sea-level rise on Bangladesh, 92 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 Areas of the African highlands that, though currently nonendemic, are probably vulnerable to malaria as the result of climate warming ( • ) , 98 Comparison of the maximum (o), mean ( • ) , and minimum (A) temperatures recorded within huts in deforested agricultural lands with the corresponding maximum (•), mean (•), and minimum (A) temperatures recorded within huts in forests, 99 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 The World Health Organization's estimates of mortality attributable to climate change by the year 2000, 103 Decrease in the time before an infectious mosquito can retransmit a virus or extrinsic incubation period from laboratory experiments, 109 (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 Flow scheme for a Dengue Decision Support System, 154

TABLES, FIGURES, AND BOXES

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Example from Chetumal, Mexico, of quality of imagery accessed through Google Earth, 155 Outline of data potentially included in a full-capacity Dengue Decision Support System, 157 Phylogenetic tree of West Nile virus, 163 Equine and human West Nile virus neuroinvasive disease cases, by year, United States, 164 West Nile virus activity and human neuroinvasive disease incidence per million population, by county, United States, 1999-2006, 166 Reported number of human West Nile virus disease cases, by week of symptom onset, 2006, United States, 167 Human cases of West Nile virus and St. Louis encephalitis neuroinvasive disease, by year, 1932-2006, United States, 168 Phylogenetic analysis of West Nile virus E gene sequences, by (A) year and (B) location, United States, 172 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 Resistance in Africa, 1950-2006, 182 Insecticide resistance monitoring methods, 183 Monitoring of insecticide resistance in Mozambique has resulted in several policy changes on the insecticide of choice for the country's IRS program, 185 Insecticide rotation, 186 Malaria Decision Support System, 188 Distribution of Culicoides episystems and bluetongue virus topotypes, 194 Bluetongue virus and Culicoides vector cycle, 196 Progression of bluetongue viruses emergence in Europe, 198 Overview of Red Rocks Canyon, Pinon Canyon Maneuver Site, southeastern Colorado, 206 Close-up view of rocky area in Red Rocks Canyon, Pinon Canyon Maneuver Site, southeastern Colorado, 206 Quarterly precipitation as recorded at three weather stations in or near the Pinon Canyon Maneuver Site, southeastern Colorado, 19952000, 210 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 (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

TABLES, FIGURES, AND BOXES

The 1991-1993 El Nino and some of its consequences in the southwestern United States, 215 The 1997-1998 El Nino and some of its consequences in the southwestern United States, 216 Available funding mechanisms for research, 286 BOXES Some Effects of Weather and Climate on Vector- and Rodent-Borne Diseases, 106 Key Questions for Development of Innovative, Sustainable, and CostEffective Dengue Prevention, 144

Summary and Assessment

VECTOR-BORNE DISEASES: UNDERSTANDING THE ENVIRONMENTAL, HUMAN HEALTH, AND ECOLOGICAL CONNECTIONS Vector-borne infectious diseases, such as malaria, dengue fever, yellow fever, and plague, cause a significant fraction of the global infectious disease burden; indeed, nearly half of the world's population is infected with at least one type of vector-borne pathogen (CIESIN, 2007; WHO, 2004a). Vector-borne plant and animal diseases, including several newly recognized pathogens, reduce agricultural productivity and disrupt ecosystems throughout the world. These diseases profoundly restrict socioeconomic status and development in countries with the highest rates of infection, many of which are located in the tropics and sub tropics. From the perspective of infectious diseases, vectors are the transmitters of disease-causing organisms; that is, they carry pathogens from one host to another.1 By common usage, vectors are normally considered to be invertebrate animals, usually arthropods, but they may also include fomites, which are defined as "[a]ny inanimate object that may be contaminated with disease-causing microorganisms and thus serves to transmit disease" (Hardy Diagnostics, 2007), or rodents, which

The Forum's role was limited to planning the workshop, and the workshop summary report has been prepared by the workshop rapporteurs as a factual summary of what occurred at the workshop. 'The variations in efficiency of disease transmission in vectors fluctuates with climate and other environmental conditions. While this is an extremely important topic in epidemiology, it was not a major topic at this workshop.

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carry the agent from a reservoir2 to a susceptible host. Vectors of human disease are typically species of mosquitoes and ticks that are able to transmit viruses, bacteria, or parasites to humans and other warm-blooded hosts. For the purposes of this discussion, a disease that is transmitted to humans, plants, or animals by any agent, arthropod, or fomite is a vector-borne disease. Over the past 30 years—following decades during which many mosquitoborne human illnesses were controlled in many areas through the use of habitat modification and pesticides—malaria and dengue fever have reemerged in Asia and the Americas, West Nile virus (WNV) has spread rapidly throughout the United States3 following its 1999 introduction in New York City, and chikungunya fever has resurged in Asia and Africa and emerged in Europe (Gubler, 1998, 2007; Roos, 2007; Yergolkar et al., 2006). The world has also recently witnessed the emergence and spread of Lyme and other tick-borne diseases (Barbour and Fish, 1993), including bluetongue (a devastating viral disease, transmitted to ruminant livestock by insect vectors, that first appeared in northern Europe in 2006),4 and the citrus tristeza virus (an aphid-borne disease that has killed tens of millions of citrus trees worldwide, and which currently threatens California orange crops) (Chung and Brlansky, 2006; Bar-Joseph et al, 1989). The considerable economic, ecological, and public health impacts of vectorborne diseases are expected to continue, given limited domestic and international capabilities for detecting, identifying, and addressing likely epidemics.5 Much remains to be discovered about the biology of these diseases, and in particular about the complex biological and ecological relationships that exist among pathogens, vectors, hosts, and their environments. Such knowledge is essential to the development of novel and more effective intervention and mitigation measures for vector-borne diseases. The Forum on Microbial Threats of the Institute of Medicine (IOM) convened a public workshop in Fort Collins, Colorado, on June 19 and 20, 2007, in order to examine the global burden of vector-borne diseases of humans, animals, and plants, and to discuss prospects for successful mitigation and response strategies. Through invited presentations and discussions, participants explored the biological and ecological context of vector-borne diseases; their health and economic impacts; emerging domestic and global diseases; public, animal, and 2 A reservoir is a source from which an infectious agent may be disseminated, such as the deer mouse being a reservoir host for hantavirus (Hardy Diagnostics, 2007). 3 And Mexico and Canada, as well. 4 See Osburn in Chapter 2 and http://www.iah.bbsrc.ac.uk/John_Gloster_3apr07.htm. 5 An epidemic, often synonymous with an outbreak, is the occurrence of more cases of disease (or injury, or any other health condition) than expected in a given area or among a specific population during a particular period. Outbreaks are sometimes defined as highly localized epidemics. Pandemics are epidemics that occur in multiple countries or continents, usually affecting a substantial proportion of the population (HHS, 2006).

SUMMARY AND ASSESSMENT

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plant health preparedness; prevention, control, and therapeutic measures; scientific and technological advances; and integration strategies to address current and future threats. ORGANIZATION OF THE WORKSHOP SUMMARY This workshop summary was prepared for the Forum membership in the name of the rapporteurs and includes a collection of individually authored papers and commentary. Sections of the workshop summary not specifically attributed to an individual reflect the views of the rapporteurs and not those of the Forum on Microbial Threats, its sponsors, or the IOM. The contents of the unattributed sections are based on the presentations and discussions at the workshop. The workshop summary is organized into chapters as a topic-by-topic description of the presentations and discussions that took place at the workshop. Its purpose is to present lessons from relevant experience, to delineate a range of pivotal issues and their respective problems, and to offer potential responses as described by workshop participants. Although this workshop summary provides an account of the individual presentations, it also reflects an important aspect of the Forum philosophy. The workshop functions as a dialogue among representatives from different sectors and allows them to present their beliefs about which areas may merit further attention. The reader should be aware, however, that the material presented here expresses the views and opinions of the individuals participating in the workshop and not the deliberations and conclusions of a formally constituted IOM study committee. These proceedings summarize only the statements of participants in the workshop and are not intended to be an exhaustive exploration of the subject matter or a representation of consensus evaluation. THE VECTOR-BORNE DISEASE THREAT: PAST, PRESENT, AND FUTURE Resurgence and Emergence of Human Vector-Borne Diseases Infectious diseases transmitted by insects and other animal vectors have long been associated with significant human illness and death. In the 17th through early 20th centuries, human morbidity and mortality due to vector-borne diseases outstripped that from all other causes combined (Gubler, 1998). The early 20th century discovery that mosquitoes transmitted diseases such as malaria, yellow fever, and dengue led quickly to the draining of swamps and ditches where mosquitoes bred, and eventually to the use of pesticides, which reduced populations of these disease vectors. The adoption of vector control measures, including the

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VECTOR-BORNE DISEASES

application of a variety of environmental management tools and approaches,6 coupled with improvements in general hygiene, enabled much of the world to experience decades of respite from major vector-borne diseases in the first half of the 20th century. This success proved fleeting, however, and vector control programs waned due to a combination of factors including the development of pesticide resistance or—sometimes doomed by their own success—the loss of financial support when vector-borne diseases were no longer perceived as an important public health threat. Today, vector-borne diseases are once again a worldwide concern and a significant cause of human morbidity and mortality, as Figure SA-1 illustrates (WHO, 2004c). Table SA-1 lists the disease burden (calculated in disabilityadjusted life years, or DALYs) associated with each of several major human vector-borne diseases (WHO, 2004b). Malaria accounts for the most deaths by far of any human vector-borne disease. The causative agents, Plasmodium spp., currently infect approximately 300 million people and cause between 1 and 3 million deaths per year, mainly in subSaharan Africa (Breman, 2001). As described by keynote speaker Duane Gubler, of the University of Hawaii, malaria provides a particularly dramatic example of vector-borne disease reemergence (Gubler, 1998). As stated by Scott and Morrison (see Chapter 2), when done properly, vector control is a well-documented and effective strategy for prevention of mosquito-borne disease. Familiar examples of successful mosquito vector interventions include: the worldwide reduction of malaria in temperate regions and parts of Asia during the 1950s and 1960s (Curtis, 2000; Rugemalila et al., 2006); yellow fever during construction of the Panama Canal; yellow fever throughout most of the Americas during the 1950s and 1960s (Soper, 1967); dengue in Cuba and Singapore (Ooi et al., 2006); and more recently, dengue in parts of Vietnam (Kay and Nam, 2005). Following the drastic depopulation of its vector, the anopheline mosquito, in the first half of the 20th century, malaria began its resurgence in Asia in the late 1960s. In Sri Lanka, where only 17 cases of malaria were reported in 1963, an epidemic of more than 440,000 cases erupted 5 years later after preventive vector control strategies were replaced with case-finding and drug treatment. Similarly, by the mid-1970s, millions of new post-control cases had occurred in India. In Africa, a recent upsurge in infection, punctuated by several major epidemics, has erupted in endemic areas (Nchinda, 1998). Explosive epidemics have also marked the resurgence of plague, dengue, and yellow fever, a situation that Gubler characterized as particularly worrisome. ''Some of these approaches include improvements in drainage and sanitation systems; filling standing water areas (pits/ponds/lagoons/irrigation ditches, etc.) that can be breeding sites for vector larvae; and the use of treated mosquito nets and covering of domestic water tanks and other potable water sources. The effective application of these environmental control measures greatly reduces the reliance on pesticides for vector control (Center for Science and Environment, 1999).

0 o

VBD Deaths/million

LZU0-1 I

I 1-20 I 20-50 50-200 200-500 500-1,900 No data

Estimates by WHO sub-region for 2002 (WHO World Health Report, 2004). The boundaries shown on this map do not imply the expression of any opinion whatsoever on the part of the World Health Organization concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimination of its frontiers or boundaries. Dotted lines on maps represent approximate border lines for which there may not yet be full agreement. © WHO 2005. All rights reserved.

FIGURE SA-1 Deaths from vector-borne diseases. SOURCE: Reprinted with permission from the World Health Organization (2004c). Oi

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VECTOR-BORNE DISEASES

TABLE SA-1 Estimates of the Global Burden of Disease Caused by Major Vector-Borne Diseases Disease

Million DALYs0

Mosquito-borne infections Malaria Lymphatic filariasis Dengue Japanese encephalitis

46.5 5.8 0.62 0.71

Others* Onchocerciasis Leishmaniasis African trypanosomiasis Chagas disease

0.48 2.1 1.5 0.67

DALY = disability-adjusted life year. "Total of DALYs for these diseases represent 17 percent of the global disease burden due to parasitic and infectious diseases. ''Synanthropic* flies play a major role in the transmission of trachoma and diarrhoeal diseases, but the attributable burden is not readily estimated; other arboviruses and typhus organisms may be of major public health significance but accurate data are not available. Animals that live in close association with humans (Montana State University Entomology Group, 2007). SOURCE: Reprinted from Townson et al. (2005) with permission from the World Health Organization.

Plague is carried by rodent fleas, which transmit the pathogen Yersinia pestis when they bite animals or humans (CDC, 2005a). Millions of people in Europe died from plague in the Middle Ages; today, antibiotics are effective against plague when administered promptly following infection. A 1994 plague epidemic in Surat, India, produced one of the first health emergencies that had a major documented impact on the global economy,7 Gubler said. When inadequate public health and government response to initial cases led to panic, nearly a quarter of the city's population fled Surat to other Indian towns and cities, carrying the disease with them. For the first time in 33 years, the World Health Organization (WHO) implemented the International Health Regulations (IHR) to contain the potential pandemic, resulting in a ban on shipping and travel that cost India an estimated $3 billion and the global economy nearly twice that sum. Dengue's resurgence has been marked not only by epidemics, but also by the emergence of a more severe form of disease, dengue hemorrhagic fever (DHF) (Gubler, 1998). Ecological disruption in Southeast Asia, brought on by World 7 The 1918-1919 influenza pandemic undoubtedly had worldwide economic repercussions; however, little data are available quantifying the immediate and long-term economic consequences of this disease event.

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SUMMARY AND ASSESSMENT 1,000,000900,000 800,000 to 700,000 a)