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Vector-Borne Disease Emergence and Resurgence

OVERVIEW

The once limited geographic and host ranges of many vector-borne diseases are expanding, spurred largely by anthropogenic factors. Epidemics of malaria, dengue, and other formerly contained vector-borne diseases are on the rise in the developing world, and in recent years the United States has witnessed the introduction of West Nile virus (WNV) in New York City and the emergence of previously unknown Lyme disease. Contributors to this chapter examine global, regional, and local phenomena associated with the emergence and resurgence of these and other vector-borne diseases, and explore the use of such information to predict future outbreaks and anticipate the geographic spread of vectors and pathogens.

The chapter begins with a summary of the workshop’s keynote address, which was presented by Duane Gubler of the University of Hawai‘i. Gubler describes the “dramatic global reemergence of epidemic vector-borne diseases” of the past three decades, in parallel with influential demographic, economic, and societal trends. He considers the changing epidemiology of malaria, plague, dengue, yellow fever, and WNV, identifies key factors in the emergence and spread of vector-borne disease, and discusses the implications of these trends for public health. In particular, he notes that advances in transportation, which centuries ago removed infectious disease barriers between the Old and New Worlds (that is, the eastern and western hemispheres), now drive the rapid, global dispersion of pathogens and their vectors. “If we hope to reverse the trend of emerging and reemerging infectious diseases,” Gubler insists, “the movement of pathogens and arthropod vectors via modern transportation must be addressed.”



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1 Vector-Borne Disease Emergence and Resurgence OVERVIEW The once limited geographic and host ranges of many vector-borne diseases are expanding, spurred largely by anthropogenic factors. Epidemics of malaria, dengue, and other formerly contained vector-borne diseases are on the rise in the developing world, and in recent years the United States has witnessed the introduction of West Nile virus (WNV) in New York City and the emergence of previously unknown Lyme disease. Contributors to this chapter examine global, regional, and local phenomena associated with the emergence and resurgence of these and other vector-borne diseases, and explore the use of such information to predict future outbreaks and anticipate the geographic spread of vectors and pathogens. The chapter begins with a summary of the workshop’s keynote address, which was presented by Duane Gubler of the University of Hawai‘i. Gubler describes the “dramatic global reemergence of epidemic vector-borne diseases” of the past three decades, in parallel with influential demographic, economic, and societal trends. He considers the changing epidemiology of malaria, plague, dengue, yellow fever, and WNV, identifies key factors in the emergence and spread of vector-borne disease, and discusses the implications of these trends for public health. In particular, he notes that advances in transportation, which cen- turies ago removed infectious disease barriers between the Old and New Worlds (that is, the eastern and western hemispheres), now drive the rapid, global disper- sion of pathogens and their vectors. “If we hope to reverse the trend of emerging and reemerging infectious diseases,” Gubler insists, “the movement of pathogens and arthropod vectors via modern transportation must be addressed.” 

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 VECTOR-BORNE DISEASES In his presentation on anthropogenic factors in tick-borne pathogen emer- gence, Durland Fish of Yale University focused on the “steadily increasing” presence of tick-borne disease in the northeastern United States associated with the reversal of deforestation in that region (see Summary and Assessment sub- section entitled “Reforestation and Tick-Borne Disease”). In addition to Lyme disease, which rose from obscurity to become the country’s most common vector- borne disease within the span of two decades, black-legged deer ticks (Ixodes scapularis) serve as the vector for Anaplasma phagocytophilum—a bacterium that causes a flu-like illness called human granulocytic anaplasmosis—and the protozoan Babesia microti can be spread by transfused blood from an infected human. The adults of this tick species feed exclusively on white-tailed deer; only the nymphs feed on and transmit pathogens to humans. The decline of agriculture in the northeastern United States and the subsequent reforestation of this region over the past several decades have provided an ideal habitat for increasing numbers of white-tailed deer, their attendant ticks, and the pathogens they bear. This trend may well continue and gain momentum, Fish noted, since various non-native tick- borne arboviruses could infect any of several hundred human-feeding species of ticks present in the United States. Although vector-borne plant diseases share many ecological and epidemio- logical features with their animal and human counterparts, they tend to be studied in isolation. In his contribution to this chapter, presenter Rodrigo Almeida of the University of California, Berkeley, argues that new insights on the nature of vector-borne diseases could be gained through the exchange of tools and ideas among disparate research communities. Plant systems, for example, “allow large experiments to be conducted, with multiple hosts, vector species and pathogen strains, which could be used to experimentally address ecological and evolution- ary hypotheses on pathogen range and transmission efficiency,” he explains. In describing the rise of Pierce’s disease of grapevines in California following the recent introduction of a highly efficient insect vector for a local bacterial patho- gen, Almeida explores a common pattern of vector-borne disease emergence from an agricultural perspective. The final essays in this chapter address the profound influence of climate on vector-borne disease distribution and transmission. The first, by presenter Kenneth Linthicum of the U.S. Department of Agriculture’s (USDA’s) Agricul- tural Research Service (ARS) Center for Medical, Agricultural, and Veterinary Entomology and co-authors, focuses on the effects of regional variations in tem- perature and rainfall on vector-borne disease transmission. The primary driver of global climate variability, the periodic warming of the Pacific Ocean surface known as the El Niño/Southern Oscillation (ENSO), has been linked with out- breaks of a variety of arthropod-borne diseases, the authors note. In the case of Rift Valley fever (RVF), this association was sufficiently strong to permit them to develop risk maps that successfully predicted a major outbreak in Africa in

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 VECTOR-BORNE DISEASE EMERGENCE AND RESURGENCE 2006-2007, providing an early warning that reduced the impact and spread of the disease. Such forecasts, they conclude, may potentially predict risk for the spread of diseases on a global scale and offer health and agricultural authorities the possibility of targeting disease surveillance and control efforts, and thereby improve their cost-effectiveness. Two consecutive contributions, from workshop speaker Jonathan Patz, of the University of Wisconsin, Madison, and co-authors, discuss the possible effects of global climate change on vector-borne disease emergence. The first paper, by Patz and S. H. Olson, comprises an overview of the effects of climate change on disease risk at both global and local levels. It is followed by an update, by Patz and C. K. Uejio, which presents detailed evidence for the effects of climate change on Lyme disease and WNV, the two most prevalent vector-borne diseases in North America. Vector-borne pathogens are particularly sensitive to climatic conditions due to their influence on vector survival and reproduction, biting and feeding patterns, pathogen incubation and replication, and the efficiency of pathogen transmis- sion among multiple hosts. The authors discuss evidence that an overall rise in global temperatures could enlarge the geographic range of malaria in Africa and increase the frequency of dengue outbreaks worldwide, but they place greater emphasis on opportunities for disease emergence in local environments driven by land use practices such as deforestation, cultivation, and dam construction. Given these influences, risk assessments for vector-borne diseases should incor- porate appropriately scaled analyses of the effects of land use on microclimate and weather, habitat, and biodiversity, the authors conclude. The need for such considerations is clearly illustrated in their discussion of WNV distribution and transmission dynamics, which appear to be influenced by a broad and complex range of environmental factors. THE GLOBAL THREAT OF EMERGENT/REEMERGENT VECTOR-BORNE DISEASES Duane J. Gubler, Sc.D. University of Hawai‘i, Honolulu, Hawai‘i Introduction At the beginning of the 20th century, epidemic vector-borne diseases were among the most important global public health problems (Gubler, 1998, 2002a). 1 Director, Asia-Pacific Institute for Tropical Medicine and Infectious Diseases; Professor and Chair, Department of Tropical Medicine, Medical Microbiology and Pharmacology, John A. Burns School of Medicine.

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 VECTOR-BORNE DISEASES Diseases such as yellow fever (YF), dengue fever (DF), plague, louse-borne Typhus, malaria, etc., caused explosive epidemics affecting thousands of people. Subsequently, other vector-borne diseases were identified as major causes of disease in both humans and domestic animals. As the natural history of these diseases became better understood, prevention and control measures, primarily directed at the arthropod vectors, were highly successful in controlling disease transmission. Effective prevention and control accelerated in the post-World War II years with the advent of new insecticides, drugs, and vaccines. By the 1960s, the majority of important vector-borne diseases had been effectively controlled in most parts of the world, and those that were not yet controlled were targeted for more intensive programs using new vaccines, drugs, and insecticides. Unfortunately, “success led to failure”; some of the successful programs, such as the Aedes aegypti eradication program that effectively controlled epi- demic YF and DF throughout the American tropics for over 40 years, and the global malaria eradication program that effectively controlled malaria in Asian and American countries, were disbanded in the 1970s because the diseases were no longer major public health problems (Gubler, 1989, 2004; Gubler and Wilson, 2005; IOM, 1992). Additionally, residual insecticides were replaced with less effective chemicals used as space sprays to control adult mosquitoes. The 1970s ushered in a 25-year period characterized by decreasing resources for infec- tious diseases, decay of the public health infrastructure to control vector-borne diseases, and a general perception that vector-borne diseases were no longer important public health problems. Coincident with this period of complacency, however, was the development of global trends that have contributed to the reemergence of epidemic infectious diseases in general, and vector-borne dis- eases in particular, in the past 25 years. In addition to the emergence of newly recognized diseases, there was increased incidence and geographic expansion of well-known diseases that were once effectively controlled (Gubler, 1989, 1998; IOM, 1992, 2003; Mahy and Murphy, 2005). This paper will briefly review the changing epidemiology of several of the most important vector-borne diseases and discuss the lessons learned from this global reemergence. The Reemergence of Epidemic Vector-Borne Diseases as Public Health Problems The earliest indications that epidemic vector-borne diseases might reemerge came in the early 1970s. Subsequent warnings were ignored by public health officials and policy makers because of competing priorities for limited resources (Gubler, 1980, 1987, 1989; IOM, 1992). The 1980s ushered in a period with increased epidemic vector-borne disease activity associated with expanding geo- graphic distribution of both the vectors and the pathogens via modern transporta- tion and globalization. It was not until the Institute of Medicine (IOM) report on emerging infectious diseases that policy makers took notice (IOM, 1992), and not

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 VECTOR-BORNE DISEASE EMERGENCE AND RESURGENCE until after the 1994 plague epidemic in India that new resources were allocated to emerging infectious diseases (Fritz et al., 1996; WHO, 1994). Parasitic, bacterial, and viral pathogens may be transmitted by blood-sucking arthropods. Mosquitoes, which primarily transmit parasitic and viral diseases, are the most important arthropod vectors; ticks, which primarily transmit bacteria and viruses, are next in importance. Parasitic Diseases Of the parasitic infections transmitted by arthropods, malaria is by far the most important, although there has also been a reemergence of leishmaniasis and African trypanosomiasis. The principal problem area for malaria is Africa, where 95 percent of all global cases occur, most of them in children under 5 years of age (Gubler and Wilson, 2005). This disease is dealt with elsewhere and will not be considered further here. Bacterial Diseases Two newly recognized vector-borne bacterial diseases, Lyme disease, caused by Borrelia burgdorferi, and ehrlichiosis, caused by Ehrlichia chaffeensis, Anaplasma phagocytophilum, and Ehrlichia ewingui, have emerged as important public health problems in the past three decades (Dumler et al., 2007; Steere et al., 2004). Both have small rodents as their natural vertebrate reservoir host, with hard ticks as their principal vectors. Both diseases are found primarily in temperate regions of the world, where emergence has been associated with environmental change. Figure 1-1 shows the dramatic increase in reported cases of Lyme disease in the United States since the Centers for Disease Control and Prevention (CDC) began surveillance in 1982. The increased transmission in the United States is directly related to reforestation of the northeastern United States, allowing the mouse and deer populations to increase unchecked, which in turn has allowed the tick population to increase. A final factor has been the trend in recent decades to build houses in woodlots where humans share the ecology with deer, mice, and ticks; thus most transmission to humans in the northeastern United States where the majority of cases of Lyme disease occur, is residential (Steere et al., 2004). Plague, caused by Yersinia pestis, is the most important reemergent bacte- rial vector-borne disease. The current global increase in case reports of plague is primarily due to outbreaks in Africa. However, it is the potential of plague to cause explosive epidemics of pneumonic disease, transmitted person-to-person and with high mortality, that makes it important as a reemergent infectious dis- ease and as a potential bioterrorist threat. This was illustrated in 1994 when an outbreak of plague occurred in Surat, Gujarat, India (WHO, 1994). Although this was a small outbreak (most likely less than 50 cases) that should have been

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 VECTOR-BORNE DISEASES 25,000 20,000 15,000 Cases 10,000 5,000 0 1982 1984 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 Year FIGURE 1-1 Reported Lyme disease cases by year, United States, 1982-2005. SOURCE: Adapted from Gubler (1998) and CDC (2006), courtesy, Division of Vector- Borne Infectious Diseases, CDC, Fort Collins, CO. fig 1-1 a relatively unimportant local public health event, it became a global public health emergency. The reasons for this are complicated and beyond the scope of this article, but it is a classic case of “success breeding failure.” Briefly, because the Indian Health Service had successfully controlled epidemic plague in India for over 30 years (the last confirmed human plague case prior to 1994 was in 1966), laboratory, clinical, and epidemiologic capacity to diagnose and control plague had deteriorated. Thus, when the Surat outbreak occurred, the clinical and laboratory diagnosis was confused, creating lack of confidence in public health agencies and ultimately panic when it was finally announced that the disease was pneumonic plague. Within a few weeks in early October 1994, an estimated 500,000 people fled Surat, a city of about 2 million people at that time. Many of these people traveled to other urban areas in India, and within days, newspapers were reporting plague cases in other cities. The World Health Organization imple- mented Article 11 of the International Health Regulations (WHO, 1983) for the first time in 33 years because it was thought that people with pneumonic plague might board airplanes in India and transport the disease to other urban centers around the world (Figure 1-2). Many countries stopped air travel and trade with India and most implemented enhanced surveillance for imported plague cases via airplane travel. This was the first global emerging infectious disease epidemic that impacted the global economy since infectious diseases were controlled in the 1950s. It is estimated that this small outbreak cost India US$3 billion (John, 1999) and the global economy US$5 to $6 billion. Fortunately, there were no

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 VECTOR-BORNE DISEASE EMERGENCE AND RESURGENCE India Delhi Calcutta Madras Bombay FIGURE 1-2 Suspected spread of pneumonic plague from India, 1994. SOURCE: Courtesy, Division of Vector-Borne Infectious Diseases, CDC, Fort Collins, CO. 1-2 cases of plague exported from India (Fritz et al., 1996), but this epidemic was the “wake-up call” that modern transportation and globalization were major drivers of pandemic infectious diseases. It was this epidemic that helped stimulate in the first funding of CDC’s Emerging Infectious Disease Program. Arboviral Diseases Of the vector-borne diseases, it is the arboviruses that have become the most important causes of reemergent epidemic disease (Gubler, 1996, 2002a). In 2007, there are few places on Earth where there is no risk of infection with one or more of these viral diseases, most of which are transmitted by mosquitoes. The more important reemergent epidemic arboviral diseases are presented in Table 1-1. They include members of three families (Togaviridae, Flaviviridae, and Bunyaviridae). Three diseases—dengue fever, West Nile, and yellow fever—will be discussed as case studies to illustrate the changing epidemiology of arboviral diseases.

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 VECTOR-BORNE DISEASES TABLE 1-1 Emergent/Reemergent Arboviral Diseases of Humans • Dengue hemorrhagic fever • Yellow fever • West Nile fever • Japanese encephalitis • Chikungunya • Rift Valley fever • Alkumra fever (Kyasanui Forest disease) • Venezuelan equine encephalitis • Epidemic polyarthritis • Barmah Forest • Oropouche • California encephalitis • Crimean-Congo hemorrhagic fever West Nile Virus West Nile virus (WNV) (Flaviviridae, genus Flavivirus), an African virus, belongs to the Japanese encephalitis virus (JEV) sero-group, which includes a number of closely related viruses, including JEV in Asia, St. Louis encephalitis virus in the Americas, and Murray Valley encephalitis virus in Australia. All have a similar transmission cycle involving birds as the natural vertebrate hosts and Culex species mosquitoes as the enzootic/epizootic vectors, and all cause severe and fatal neurologic disease in humans and domestic animals, which are generally thought to be incidental hosts, as well as in birds. The clinical illness associated with WNV in humans ranges from asymptom- atic infection to viral syndrome to neurologic disease (Hayes and Gubler, 2006), but historically it has been considered among the least virulent of the Japanese encephalitis sero-group viruses (Hayes, 1988); recent epidemics, however, have changed that perception. From the time WNV was first isolated from the blood of a febrile patient in the West Nile province of Uganda in 1937 (Smithburn, 1940) until the fall of 1999, it was considered relatively unimportant as a human and animal pathogen. The virus was enzootic throughout Africa, West and Central Asia, the Middle East, and the Mediterranean, with occasional extension into Europe (Hayes, 1988). A subtype of WNV (Kunjin) is also found in Australia (Hall et al., 2002). A characteristic of WNV epidemiology during this 62-year history (1937-1999) was that it caused epidemics only occasionally, and the illness in humans, horses, 2 Reprinted in part with permission from Gubler (2008). Copyright 2008.

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 VECTOR-BORNE DISEASE EMERGENCE AND RESURGENCE and birds was generally either asymptomatic or mild; neurologic disease and death were rare (Marfin and Gubler, 2001; Murgue et al., 2001, 2002). In late August 1999, an astute physician in Queens, New York, identified a cluster of elderly patients with viral encephalitis (Asnis et al., 2000). Because of the age group involved and the clinical presentation, these cases were initially thought to be St. Louis encephalitis, but subsequent serologic and virologic investigation showed them to be caused by WNV (Lanciotti et al., 1999). The epidemic investigation, which focused only on neurologic disease, identified 62 cases with 7 (11 percent) deaths, all of them in New York City (Nash et al., 2001). Epidemiologic studies, however, showed widespread transmission throughout New York City, with thousands of infections (Montashari et al., 2001; Nash et al., 2001). The virus caused a high fatality rate in birds, especially those in the family Corvidae (Komar, 2003). Genetic sequence of the infecting virus suggested it was imported from the Middle East, most likely from Israel (Lanciotti et al., 1999). Although it will never be known for sure, epidemiologic and virologic evidence suggests the virus was introduced in the spring or early summer of 1999, most likely via infected humans arriving from Israel, which was experiencing an epi- demic of WNV in Tel Aviv at the time (Giladi et al., 2001; Marfin and Gubler, 2001). Over the next 5 years, WNV rapidly moved westward across the United States to the west coast (Figure 1-3), north into Canada, and south into Mexico, the Caribbean, and Central America. In 2002, it caused the largest epidemic of meningoencephalitis in U.S. history with nearly 3,000 cases of neurologic disease and 284 deaths. That same year, there was a large epizootic in equines with over 14,500 cases of neurologic disease and a case fatality rate of nearly 30 percent (Campbell et al., 2002). The epidemic curve for human cases in the United States is shown in Figure 1-4. In 2003, another large epidemic occurred, but the epicen- ter of transmission was in the plains states and the majority of the reported cases were not neurologic disease (Hayes and Gubler, 2006). Since 2003, the virus has persisted with seasonal transmission during the summer months, but at a lower level; the majority of cases have been in the plains and western states. WNV was first detected south of the U.S. border in 2001 when a human case of neuro-invasive disease was reported in the Cayman Islands (Campbell et al., 2002), and birds collected in Jamaica in early 2002 were positive for WNV- neutralizing antibodies (Komar and Clark, 2006). In 2002, WNV activity was reported in birds and/or equines in Mexico (in six states) and on the Caribbean islands of Hispaniola (Greater Antilles) and Guadeloupe (Lesser Antilles). Most likely, the virus was also present in Mexico in 2001, since a cow with WNV- neutralizing antibody was detected in the southern state of Chiapas in July of 2001 (Ulloa et al., 2003). In 2003, the virus was detected in 22 states of Mexico; in Belize, Guatemala, and El Salvador in Central America; and in Cuba, Puerto Rico, and the Bahamas in the Caribbean. In 2004, WNV activity was reported from northern Colombia, Trinidad, and Venezuela, the first reported activity in

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0 VECTOR-BORNE DISEASES FIGURE 1-3 The sequential westward movement of West Nile virus in the United States by year, reported to CDC as of January 31, 2006. Human infection was found in all states in the continental United States with the exception of Maine. SOURCE: Reprinted from Gubler (2007). South America; in 2006, Argentina reported WNV transmission (Komar and Clark, 2006; Morales et al., 2006). Migratory birds have likely played an important role in the spread of WNV in the western hemisphere (Owen et al., 2006; Rappole et al., 2000). This con- clusion is supported by data on the movement of WNV in migratory birds in the Old World (Malkinson et al., 2002). Moreover, the westward movement of WNV across the United States and Canada can best be explained by introduction via migratory birds that fly south to Central and South America in the fall and north from those areas in the spring. Thus, the yearly movement westward in 2000, 2001, 2002, 2003, and 2004 shows very good correlation with the Atlantic, Mississippi, Central, and Pacific flyways of migratory birds (Figures 1-3 and 1-5). After introduction to an area, local dispersion of WNV likely occurred via movement of resident birds, which often fly significant distances. Interestingly, the major epidemic in each region of the country occurred the following year after introduction, with the exception of the 1999 New York outbreak. The emergence of a WNV strain with greater epidemic potential and viru-

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 VECTOR-BORNE DISEASE EMERGENCE AND RESURGENCE 9,850 10,000 9,000 No. of Cases Reported 8,000 7,000 6,000 5,000 4,269 4,156 4,000 2,949 2,448 3,000 2,000 1,000 62 66 21 0 99 00 01 02 03 04 05 06 19 20 20 20 20 20 20 20 Year FIGURE 1-4 Epidemic West Nile virus in the United States, 1999-2006, reported to CDC as of May 2, 2007. SOURCE: CDC (2007). 1-4 lence was likely a major factor in the spread of WNV in both the Old and the New Worlds (Marfin and Gubler, 2001). The first evidence of this new strain of WNV was in North Africa in 1994, when an epidemic/epizootic of serologically confirmed WNV occurred in Algeria; of 50 cases with neurologic disease 20 (40 percent) were diagnosed as encephalitis and 8 (16 percent) died (Murgue et al., 2002). Over the next 5 years, epidemics/epizootics occurred in Morocco, Romania, Tunisia, Israel, Italy, and Russia, as well as jumping the Atlantic and causing the epidemic in Queens, New York (Figure 1-6). All of these epidemics/ epizootics were unique from earlier epidemics in that they were associated with a much higher rate of severe and fatal neurologic disease in humans, equines, and/or birds. This virus most likely had better fitness and caused higher vire- mias in susceptible hosts, allowing it to take advantage of modern transportation and globalization to spread, first in the Mediterranean region and Europe, and then to the western hemisphere. This speculation is supported by sequence data documenting that the viruses isolated from these recent epidemics/epizootics are closely related genetically, most likely having a common origin; all belonged to the same clade (Lanciotti et al., 1999, 2002) (Figure 1-7). Moreover, experimental infection of birds has documented that viruses in this clade, represented by the

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