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 subtropics.

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.

1

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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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 agricul- tural 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 subtropics. 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. 1The 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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 VECTOR-BORNE DISEASES 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 mosquito- borne 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 vector- borne 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 patho- gens, 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) con- vened 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, ani- mals, 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 2A 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). 3And Mexico and Canada, as well. 4 See Osburn in Chapter 2 and http://www.iah.bbsrc.ac.uk/John_Gloster_3apr07.htm. 5An 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).

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 SUMMARY AND ASSESSMENT plant health preparedness; prevention, control, and therapeutic measures; scien- tific 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 mos- quitoes 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 disability- adjusted 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 dis- ease. The causative agents, Plasmodium spp., currently infect approximately 300 million people and cause between 1 and 3 million deaths per year, mainly in sub- Saharan 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. 6 Some of these approaches include improvements in drainage and sanitation systems; filling stand- ing 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 reli- ance on pesticides for vector control (Center for Science and Environment, 1999).

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Deaths from vector-borne disease VBD Deaths/million 0-1 1-20 20-50 Estimates by WHO sub-region for 2002 (WHO World Health Report, 2004). 50-200 The boundaries shown on this map do not imply the expression of any opinion whatsoever on the 200-500 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 500-1,900 represent approximate border lines for which there may not yet be full agreement. No data © WHO 2005. All rights reserved. FIGURE SA-1 Deaths from vector-borne diseases. SOURCE: Reprinted with permission from the World Health Organization (2004c).  `SA-1 Landscaspe view

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 VECTOR-BORNE DISEASES TABLE SA-1 Estimates of the Global Burden of Disease Caused by Major Vector-Borne Diseases Million DALYsa Disease Mosquito-borne infections Malaria 46.5 Lymphatic filariasis 5.8 Dengue 0.62 Japanese encephalitis 0.71 Othersb Onchocerciasis 0.48 Leishmaniasis 2.1 African trypanosomiasis 1.5 Chagas disease 0.67 DALY = disability-adjusted life year. aTotal of DALYs for these diseases represent 17 percent of the global disease burden due to para- sitic and infectious diseases. bSynanthropic* 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 pub- lic 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 7The 1918-1919 influenza pandemic undoubtedly had worldwide economic repercussions; how- ever, little data are available quantifying the immediate and long-term economic consequences of this disease event.

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 SUMMARY AND ASSESSMENT 1,000,000 900,000 800,000 700,000 Number of Cases 600,000 500,000 400,000 300,000 200,000 100,000 0 9 9 9 9 9 5 95 96 97 98 99 00 -1 -1 -1 -1 -1 -2 55 60 70 80 90 00 19 19 19 19 19 20 Year FIGURE SA-2 Dengue/dengue hemorrhagic fever, average annual number of cases reported to WHO, 1955-2005. SOURCE: Courtesy of WHO. SA-2 War II, led to increased transmission of dengue and, eventually, a pandemic. As illustrated in Figure SA-2, dengue/DHF is one of the world’s fastest-growing vector-borne diseases (see Gubler in Chapter 1) (WHO, 2007a). 8 The summer of 2007 brought the worst dengue epidemic in nearly a decade to Asia (Mason, 2007). By July—well before transmission was expected to have peaked—Indonesia alone had experienced over 100,000 infections and 1,100 deaths. The epidemic was apparently spurred by weather conditions: a period of drought, during which water stored around homes provided an ideal habitat for mosquitoes to breed. This was followed by unusually hot, humid weather, in which adult mosquitoes thrive (ProMed-Mail, 2007; Anyamba et al., 2006). Yellow fever, which along with dengue was controlled in the Americas by a variety of mosquito abatement techniques through the mid-20th century, remains 8 However, chikungunya, hantavirus pulmonary syndrome, and Lyme disease may have a higher percentage of new cases based on local populations that are immunologically naïve being exposed to and acquiring these newly emerging diseases (IOM, 2003; Chretien et al., 2007).

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 VECTOR-BORNE DISEASES a constant threat, with concerns that it might make its first appearance in Asia (see Gubler in Chapter 1). Yellow fever virus has caused major epidemics in Africa and South America (Gubler, 2001; Monath, 2001), and sylvatic reservoirs in these areas provide an ongoing threat for its reintroduction into Aedes aegypti- infested metropolitan areas throughout the world. Ae. aegypti is also the principal vector of the dengue viruses (IOM, 2003). The virus was apparently carried by infected birds (and possibly mammals as well) abetted by a vast and diverse population of mosquitoes (see Gubler in Chapter 1 and Petersen in Chapter 2). Indeed, Gubler concluded, nearly all of the most important vector-borne human diseases have exhibited dramatic changes in incidence and geographic range in recent decades. Impact of Vector-Borne Animal and Plant Diseases The majority of emerging, reemerging, and novel human infectious diseases are zoonoses (diseases that can be transmitted from animal reservoirs to humans), of which vector-borne diseases comprise a large percentage (IOM, 2003). Rift Valley fever (RVF), an acute mosquito-borne viral disease, primarily affects live- stock (e.g., cattle, buffalo, sheep, goats) but can also be transmitted to humans through direct contact with the tissues or blood of infected animals, as well as by mosquito bites (see Linthicum et al. in Chapter 1 and Peters in Chapter 2) (CDC, 2007a). Outbreaks of RVF among animals can spread to humans; the largest reported human outbreak, which occurred in Kenya during 1997-1998, resulted in an estimated 89,000 infections and 478 deaths (CDC, 2007b). African try- panosomiasis, also known as African sleeping sickness, causes estimated losses in cattle production of more than $1 billion per year, and perhaps five times that amount in lost opportunities for development (FAO, 2007a). The disease currently affects an estimated 500,000 people in sub-Saharan Africa but threatens an esti- mated human population of 60 million, as well as 50 million head of cattle (FAO, 2007a). Given the rapid growth of human and domesticated animal populations, and their increasing contact with each other and with wild animals, the zoonotic disease threat is expected to increase (Karesh and Cook, 2005; Murphy, 1998; NRC, 2005). Vector-borne diseases have the potential to cause enormous economic harm when they affect livestock and crops, and even the threat of infection can severely limit trade. For example, bluetongue, a viral disease transmitted among sheep and cattle by biting midges, results in annual losses of approximately $3 billion due to morbidity and mortality of animals, trade embargoes, and vaccination costs (see Osburn in Chapter 2) (FAO, 2007b; Osburn, 2007). Although considerable attention and resources have been committed to agriculturally important vector- borne diseases such as bluetongue, RVF, and African trypanosomiasis, relatively little is known about the vast majority of vector-borne disease-causing organ- isms that currently infect only wild animals. Yet such diseases can disrupt entire

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 SUMMARY AND ASSESSMENT ecosystems and, under the right conditions, could potentially expand their host range to include livestock, pets, or humans (Marin/Sonoma Mosquito and Vector Control District, 2005). Vector-borne plant diseases profoundly affect agricultural productivity and ecosystem dynamics (Gergerich and Dolja, 2006; Purcell, 1982; Weintraub and Beanland, 2006). Examples include the bacterium, Xylella fastidiosa, which damages a wide range of plant species; in grapevines, it causes Pierce’s disease, a significant threat to California’s table grape and wine industries (see Almeida in Chapter 1) (Fletcher and Wayadande, 2002; NRC, 2004). Emerging vector- borne viral and bacterial diseases of citrus, most of which were introduced into the Americas since 2000, threaten 85 percent of the world’s orange juice produc- tion, which resides in the United States and Brazil (Almeida, 2007; Woodall, 2007). Due in part to the difficulty of discerning whether damage to plants has been caused by disease, insects, or adverse weather conditions, the overall impact of vector-borne plant diseases cannot be accurately estimated (Almeida, 2007; Gergerich and Dolja, 2006); however, annual losses in crop quality and yield associated with certain vector-borne viruses are measured in the billions of dol- lars (Bowers et al., 2001; Gergerich and Dolja, 2006; Hull, 2002; Sherwood et al., 2003). Vector-borne plant diseases also cause immeasurable damage to ecosystems, which may not be recognized until it threatens human health, safety, or prosperity. For example, Sudden Oak Death (SOD)—an emerging infectious disease that has been spread across wild lands by hikers, mountain bikers, and equestrians (i.e., human “vectors”)—was recognized after it caused widespread dieback of several tree species in West Coast forests (see subsequent section, “Lessons Learned: Case Studies of Vector-Borne Diseases” and Chapter 2) (California Oak Mortality Task Force, 2004; Rizzo and Garboletto, 2003). These losses are likely to reduce shelter and food sources for wildlife, increase fire frequency and intensity, and compromise water quality due to soil surface exposure. Moreover, such ecologi- cal effects can be long-lasting. For example, changes in forest composition in the Canadian Rocky Mountains, which resulted from the deaths of lodgepole pines due to an infestation of bark beetles, have persisted for as long as 65 years (Cur- rent Results, 2007; Dykstra and Braumandl, 2006). Back to the Future Infectious diseases have always accompanied humans, animals, plants, and goods in their travels. “Since the beginning of recorded history, disease epidemics have been associated with trade,” Gubler observed, noting that the plague epi- demic that killed one in every four Europeans in the 14th century is believed to have been introduced to the continent by commercial trade with Asia. The rapid expansion of global trade and transportation since 1700 has been associated with the spread of mosquito-borne diseases such as yellow fever and dengue. Dutch

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0 VECTOR-BORNE DISEASES Elm disease (so named because it was first described in Holland, in 1921) also originated in Asia and probably arrived in the United States on a shipment of lumber from Europe in the 1930s, after which it devastated American elms in forests and on city streets (Plant Disease Diagnostic Clinic, Cornell University, 2005; Riveredge Farms, 2004). Today’s integrated global economy has accelerated the transnational flow of capital, knowledge, people, livestock and animal products, and plant materials, as well as the introduction of pathogens and their vectors to new hosts and geo- graphic ranges. Presented with these opportunities, several vector-borne diseases considered most problematic 100 years ago, such as malaria, dengue, plague, and yellow fever, once again pose serious threats to public health. While we have gained considerable insights into the biology and management of certain vector-borne diseases over the past century, limited capacity exists to apply that knowledge. In addition, as many workshop participants observed, much remains to be learned about the ecology and epidemiology of a broad spectrum of vector- borne diseases, including those that have recently emerged. Subsequent sections of this summary therefore explore both what we know and what we most need to understand about the biology of vector-borne diseases, the factors that precipitate disease emergence and resurgence, discussion about key research areas needed to fill the current gaps, and strategies for disease detection and response. HALLMARKS OF VECTOR-BORNE DISEASE Vector-borne diseases are transmitted among their human, animal, or plant hosts by arthropods,9 usually insects. A broader definition of vector-borne disease recognizes that other animals can serve in the role of infectious disease vector by harboring pathogens that cause disease only in susceptible populations. These unconventional “reservoirs” include invertebrates other than arthropods (e.g., snails, in the case of schistosomiasis), rodents (which spread a variety of viral diseases, including hantavirus pulmonary syndrome [HPS]), and even humans (as noted earlier in the case of SOD). Mosquitoes, ticks, and biting flies spread viruses, bacteria, and parasites within and among a variety of warm-blooded hosts. Arthropod-borne viruses (arboviruses) comprise the largest class of vector-borne human pathogens; over 500 arboviruses have been described, 20 percent of which are known to cause human disease (Gray and Banerjee, 1999; Gubler, 1998; Jacobson, 2007). These include dengue and DHF, yellow fever, RVF, and WNV (one among a number of arboviral causes of encephalitis) (CDC, 2005b; Gubler, 1998; WHO, 2005). Vector-pathogen relationships are central to the epidemiology of many 9Arthropods (members of the phylum Arthropoda) are invertebrates with jointed limbs, segmented bodies, and exoskeletons made of chitin. They include insects, spiders, crustaceans (e.g., shrimp, lobsters), and centipedes.

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 SUMMARY AND ASSESSMENT important plant diseases (Gergerich and Dolja, 2006; Purcell, 1982; Weintraub and Beanland, 2006). While only certain bacterial pathogens of plants require a vector for transmission, most plant viruses are spread from infected to uninfected plants via a plant-feeding arthropod, or nematode. Several important bacterial pathogens are delivered directly into the plants’ vasculature—either the sugar- transporting phloem or water-transporting xylem networks—by insects that feed on plant vascular fluids (Fletcher and Wayadande, 2002). Workshop participants reflected upon the breadth and diversity of vector- borne diseases of humans, animals, and plants, but also sought to identify com- monalities within and among them and to highlight the unique challenges these diseases present to science, agriculture, public health, and domestic animal and wildlife health. These discussions focused on the vector’s paramount importance to the ecology and epidemiology of vector-borne diseases, a role which compli- cates transmission patterns, but which also provides opportunities for disease control. Dynamics of Disease Transmission A standard graphic representation of the ecology of infectious disease fea- tures host, pathogen, and environment as circles intersecting in a common zone that defines permissive conditions for disease transmission (see Figure SA-3). The ecology and epidemiology of vector-borne diseases are particularly complex and often involve multiple disease cycles through alternate vectors and hosts, noted presenter Rodrigo Almeida of the University of California, Berkeley (see Chapter 1). His octagonal model, shown in Figure SA-4, depicts key influ- ences on vector-borne plant disease; a similar diagram could illustrate the web of relationships governing animal and human vector-borne diseases. The inherently complex ecologies of individual vector-borne diseases are discussed in several case studies collected in Chapter 2. A confluence of risk factors for a vector-borne disease may result in an outbreak, according to speaker Ned Hayes of the Centers for Disease Control and Prevention (CDC). An outbreak is a condition defined by an increase over background of disease incidence within a subpopulation of potential hosts. Epide- miologists investigating infectious disease outbreaks seek to determine the route of transmission; in the case of vector-borne diseases, their efforts necessarily focus on the presence, abundance, and ecology of the vector, which in turn may frequently be influenced by environmental conditions and human behavior. To illustrate these connections, Hayes described his experiences investigating three different vector-borne diseases in diverse settings: pneumonic plague in Ecuador, 1998; dengue at the Mexico-Texas border, 1999; and tularemia in Martha’s Vine- yard, Massachusetts, 2000 (see Chapter 2 Overview). Approximately 80 percent of vector-borne disease transmission typically occurs among 20 percent of the host population (Smith et al., 2005; Woolhouse

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0 VECTOR-BORNE DISEASES discussion therefore highlights specific challenges that originate in the definitive role of the vector in the ecology and epidemiology of this important class of human, animal, and plant infectious diseases. Integrating Disciplines and Systems In the course of a panel discussion on integrating strategies for surveillance, diagnosis, and response, the four discussants—who represented the CDC, the National Institute of Allergy and Infectious Disease of the National Institutes of Health (NIAID/NIH), and the U.S. Department of Agriculture (USDA)— emphasized the importance of multidisciplinary efforts toward understanding and addressing individual vector-borne diseases, as well as groups of diseases that share a common vector (see Chapter 3). Roger Nasci, chief of the Arbo- viral Diseases Branch at CDC’s Division of Vector-Borne Infectious Diseases, described multidisciplinary teams as “essential” to addressing international health problems, but also noted the difficulties in coordinating such teams (e.g., the previously discussed response to RVF in Kenya). Panelists described existing multidisciplinary programs of limited scope, such as CDC field teams that respond to vector-borne outbreaks and research groups that address West Nile encephalitis and plague (see Nasci in Chapter 3), and advocated a wider adoption of this approach. “We have to provide an environ- ment to foster [multidisciplinarity] in training, as well as in research,” said David Morens of NIAID; for example, by changing the current paradigm of highly com- partmentalized Ph.D. programs and instead emphasizing interdisciplinary studies in global health (see Chapter 3) (Hotez, 2004). Similarly, Forum member Lonnie King observed that working at the interface of different scientific cultures is a learned skill that needs to be taught. Panelist Sherrilyn Wainwright (see Chapter 3), a veterinary epidemiologist with the USDA currently working at Colorado State University, suggested that involvement in multidisciplinary research trains scientists to better integrate their distinct cultures in other circumstances, such as outbreak response. Participants in the ensuing open discussion urged the expansion of multidis- ciplinary research and response and encouraged the development of “transdisci- plinary” programs that integrate diverse disciplines in a meaningful fashion, rather than simply involving representatives of different fields. Some also advocated expanding the range of disciplines brought to bear on vector-borne diseases beyond public health, ecology, and the biomedical sciences, to include professionals such as urban planners, hydrologists, ecologists, and engineers. ArboNET, a pioneer among integration disease surveillance systems, pro- vides a model for the collection and organization of information on zoonotic diseases, according to Nasci (see Chapter 3, Petersen in Chapter 2, and previous discussion in “Lessons Learned: Case Studies of Vector-Borne Diseases”). This environmental surveillance program could be harnessed for broader use, as is

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 SUMMARY AND ASSESSMENT currently being explored in an experimental ArboNET/plague surveillance system designed to test models that could provide early warning of plague outbreaks. In addition to gathering surveillance on vector-borne diseases, it would be use- ful to integrate and disseminate data that have already been accumulated, King observed, because to a large extent, “we don’t know what we know.” For example, as Nasci pointed out, data from the USDA’s equine arbovirus monitoring program could be integrated into ArboNET. Knowledge Gaps The need to understand better the ecology of vector-borne diseases, a central theme of workshop discussions (see Fish in Chapter 1), was identified as critical to a host of purposes: • Targeting surveillance and control efforts • Minimizing surveillance costs over large areas • Forecasting risk and anticipating expansion of disease range (including globalization) • Designing containment or exclusion strategies In addition, basic questions remain to be answered about most important vector-borne diseases (see Chapter 2 and Fish in Chapter 1). The following infor- mation was deemed essential by workshop presenters: • Quantitative descriptions of endemic and epidemic disease cycles in all hosts • Measurements of disease transmission potential by known and potential vectors • Timing, distribution, and abundance of disease-competent vectors • Mechanisms of host infection • Mechanisms of pathogenesis • Mechanisms of transovarial transmission • Spatial and temporal distributions of vectors and environmental condi- tions in settings at risk for disease emergence Field studies of vectors are crucial to answering many of these questions; however, as several participants who engage in such research attested, this work is not well funded. For example, Fish has written, “Some research is being done on methods for reducing the risk of Lyme disease through tick population sup- pression and other field intervention strategies, but this effort has been meager compared to that already invested in vaccines [that were withdrawn from the mar- ket]. One can only imagine what impact [the money invested in developing the discontinued Lyme vaccine, conservatively estimated at $200 million] would have

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 VECTOR-BORNE DISEASES [had] upon research to answer some basic questions about tick ecology, such as what limits the geographic distribution of Lyme disease vectors” (Fish, 2001a). Obstacles to Scientific Education and Training The introduction of WNV into the United States resulted in an unprecedented demand for expertise in mosquito surveillance and control operations throughout most of the country, Fish observed in a 2001 editorial (Fish, 2001b). However, there is a strong perception among those in the field that—after three decades of decline in mosquito-borne disease in the United States, the dismantling of train- ing programs, and a loss of employment opportunities for vector biologists and medical entomologists—positions went unfilled, and few academic institutions were capable of providing such training. The CDC briefly financed training in medical entomology at four institutions with the new funds provided to it for WNV, but that funding has since been cut, and the programs are slated for ter- mination (Fish, 2007). Panelist Adriana Costero, Vector Biology Program Officer at NIAID/NIH, described the Institute’s programs, which fund basic and translational research and training in the United States and in disease-endemic countries (see Chap- ter 3). However, several participants expressed discouragement at the lack of research funding targeted specifically for vector ecology and the resulting dearth of expertise—as well as the persistence of knowledge gaps—in this field. Various causes were postulated for this deficit, from the broad (funding trends that favor solutions to well-defined problems, preferably posed by the “disease du jour,” over descriptive studies of infectious diseases) to the specific (the organization of NIH study sections [Spielman, 2003]). However, as Forum member Stephen Morse observed, every scientific specialty complains of insufficient funding, a symptom of a scientific establishment focused on specialized research programs that compete for limited funds. Multidisciplinary approaches offer a solution to this dilemma by creating unified communities, synergies of expertise, and economies of scale commensu- rate with problems as complex and wide-ranging as the prevention and mitigation of vector-borne disease. Such efforts, it was suggested, might be most expedi- ently funded if they capitalized on the “disease du jour,” and also if they offered near-term benefits for public health (e.g., how best to use existing pesticides in disease control and prevention). Barriers to Implementation There is a general lack of infrastructure for implementing vector-borne disease interventions in most settings, Morens observed, whether they are cit- ies in the United States—as revealed by the introduction of Lyme disease—or impoverished countries where vector-borne diseases cause major morbidity and

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 SUMMARY AND ASSESSMENT mortality. “Many folks were shocked to discover [upon the arrival of WNV] that there were state health departments in the United States that had no vector people anymore,” he said. The domestic situation has improved somewhat, he added, but the same cannot be said for developing countries, where infrastructures for infec- tious disease control lack far more than vector biologists. Moreover, legal and bureaucratic barriers increasingly impede international research on and response to vector-borne disease. Because many vector-borne infectious agents have been classified as “Select Agents,” they are subject to rules associated with the USA Patriot Act21 that substantially limit the ability of foreign scientists to work on U.S.-funded research efforts even within their own countries. In addition, U.S. air transportation regulations and bans on the international transport of biological specimens by nations experiencing disease outbreaks slow and sometimes stop the vital exchange of biological materials (see Morens in Chapter 3). Meanwhile, 8 years after the introduction of WNV, the U.S. response to the threat of vector-borne disease is fading, as illustrated by recent funding reductions that will shrink the CDC’s WNV program by nearly 50 percent over the next 2 years (Fish, 2007). “These cuts will force big reductions in federal support for the surveillance and control of WNV in 57 state and local jurisdictions,” Fish noted in an editorial in the May 27, 2007, New York Times: “While federal financing for biosecurity and public health preparedness has . . . become a priority, in fact little has been learned from the WNV experience,” he continued. WNV is certainly not the last mosquito-borne virus that will invade the United States, Fish predicted, but without sustained federal support for surveillance and control of such dis- eases, “we will again be vulnerable to threats, accidental or not, and incapable of prompt action that could curb or prevent epidemics.” Reflecting on this situation, Forum member George Korch wondered aloud how governments and industry might be convinced to invest in addressing vector- borne diseases. “What is the product that medical entomology and infectious disease studies provide?” he inquired. A major common goal for countries, or cultures, is to have a productive and healthy workforce that translates into the well-being of the entire community, he suggested. Thus, in order to convince the pharmaceutical industry, as well as governments, that vector-borne diseases are worth solving, researchers will need to provide evidence of economic benefit and opportunities for strategic investment. Even training is a short-term solution unless it fits into a grand matrix of vector-borne disease control, Korch said. 21 “Uniting and Strengthening America by Providing Appropriate Tools Required to Intercept and Obstruct Terrorism (USA PATRIOT ACT) Act of 2001.” The USA PATRIOT Act (Patriot Act), Public Law 107-56, enacted by Congress and signed by the President on October 26, 2001, provides expanded law enforcement authorities to enhance the federal government’s efforts to detect and deter acts of terrorism in the United States or against United States’ interests abroad (DoJ/OIG, 2003).

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 VECTOR-BORNE DISEASES Conclusions While acknowledging the global burden of vector-borne diseases, as well as the daunting obstacles to much-needed research on their control, prevention, and treatment, Forum chairman Fred Sparling also expressed optimism and excite- ment in the pursuit of solutions. Recalling that the final recommendation in the 2003 report Microbial Threats to Health advocated the creation of interdisciplin- ary centers for infectious disease research, he applauded the development of such a center—albeit a “virtual” one—at Colorado State University, in close associa- tion with the nearby CDC Division of Vector-Borne Infectious Diseases. 22 Other universities (e.g., Vanderbilt, Duke, Johns Hopkins, and the University of Washington, Seattle23) are creating centers for global health. These initiatives are driven, in large part, by the promise of funding from the Bill and Melinda Gates Foundation and other public and private sources, Sparling said. In such a climate, and in such interdisciplinary venues, he encouraged vector biologists to look for opportunities and synergies and, thereby, support for their field. Like vector-borne diseases themselves, he concluded, research in this area is rife with thorny problems, but also abundant with opportunity. REFERENCES Almeida, R. 2007. Vector-borne plant diseases: factors driving the emergence and spread of patho- gens. Presentation at the Forum on Microbial Threats workshop entitled “Vector-borne diseases: Understanding the environmental, human health, and ecological connections,” June 19-20, 2007, Ft. Collins, CO. Anderson, P. K., A. A. Cunningham, N. G. Patel, F. J. Morales, P. R. Epstein, and P. Daszak. 2004. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends in Ecology and Evolution 19(10):535-544. Anyamba, A., J.-P. Chretien, J. Small, C. J. Tucker, and K. J. Linthicum. 2006. Developing global climate anomalies suggest potential disease risks for 2006-2007. International Journal of Health Geographics 5:60. Barbour, A. G., and D. Fish. 1993. The biological and social phenomenon of Lyme disease. Science 260(5114):1610-1616. Bar-Joseph, M., R. Marcus, and R. F. Lee. 1989. The continuous challenge of citrus tristeza virus control. Annual Review of Phytopathology 27(1):291-316. Baylis, M., P. Mellor, and R. Meiswinkel. 1999. Horse sickness and ENSO in South Africa. Nature 397(6720):574. Biggerstaff, B. J., and L. R. Petersen. 2002. Estimated risk of West Nile virus transmission through blood transfusion during an epidemic in Queens, New York City. Transfusion 42(8):1019-1026. 22 Included in this consortium are U.S. Department of Agriculture/Agriculture Research Service, U.S. Department of the Interior, and the National Wildlife Research Center, all of which are co-located in and around Ft. Collins, Colorado, for the study of vector-borne diseases. 23Although only a few are listed, there are many universities with, or in the process of creating, such centers.

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