Ecology and Geographical Expension of JE

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Ecology and Geographical Expansion of Japanese Encephalitis Virus

Andrew F. van den Hurk,1,2 Scott A. Ritchie,3,4 and John S. Mackenzie5
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Annu. Rev. Entomol. 2009.54:17-35. Downloaded from arjournals.annualreviews.org by 150.185.73.180 on 06/18/09. For personal use only.
Virology, Queensland Health Forensic and Scientic Services, Archereld, Queensland 4108, Australia; email: andrew hurk@health.qld.gov.au School of Molecular and Microbial Sciences, The University of Queensland, St. Lucia, Queensland 4072, Australia Tropical Population Health Unit Network, Queensland Health, Cairns, Queensland 4870, Australia; email: scott ritchie@health.qld.gov.au School of Public Health and Tropical Medicine, James Cook University, Cairns, Queensland 4870, Australia Australian Biosecurity Cooperative Research Center for Emerging Infectious Disease, Division of Health Sciences, Curtin University of Technology, GPO U1987, Perth, Western Australia 6845, Australia, email: J.Mackenzie@curtin.edu.au
Annu. Rev. Entomol. 2009. 54:1735 The Annual Review of Entomology is online at ento.annualreviews.org This articles doi: 10.1146/annurev.ento.54.110807.090510 Copyright c 2009 by Annual Reviews. All rights reserved 0066-4170/09/0107-0017$20.00
Key Words
avivirus, Culex, pigs, wading birds, Asia
Abstract
Japanese encephalitis virus ( JEV) (Flavivirus: Flaviviridae) is a leading cause of encephalitis in eastern and southern Asia. The virus is maintained in a zoonotic cycle between ardeid wading birds and/or pigs and Culex mosquitoes. The primary mosquito vector of JEV is Culex tritaeniorhynchus, although species such as Cx. gelidus, Cx. fuscocephala, and Cx. annulirostris are important secondary or regional vectors. Control of JEV is achieved through human and/or swine vaccination, changes in animal husbandry, mosquito control, or a combination of these strategies. This review outlines the ecology of JEV and examines the recent expansion of its geographical range, before assessing its ability to emerge in new regions, using the hypothetical establishment in the United States as a case study.
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INTRODUCTION
JEV: Japanese encephalitis virus JE: Japanese encephalitis; refers to the clinical disease in humans MVEV: Murray Valley encephalitis virus SLEV: St. Louis encephalitis virus
WNV: West Nile virus KUNV: Kunjin virus Epizootic: a period of increased virus amplication within an animal population, which can lead to incidental transmission to humans Extrinsic incubation period (EIP): the time between ingestion of the virus by the arthropod vector and transmission during a subsequent blood meal Synchronous seroconversion: where the majority of pigs seroconvert in a short period of time Asynchronous seroconversion: where seroconversion is protracted, and some animals do not display antibodies even by the end of the transmission period
Japanese encephalitis virus ( JEV) is a member of the JEV serological complex, the members of which cause signicant morbidity and mortality. The complex consists of eight species and two strains/subtypes: Japanese encephalitis ( JEV), Murray Valley encephalitis (MVEV), St. Louis encephalitis (SLEV), West Nile (WNV), Kunjin (KUNV), Alfuy, Cacipacore, Yaounde, Koutango, and Ustusu viruses (131). JEV is the most important member of the JEV group, with an estimated worldwide annual incidence of 45,000 human cases and 10,000 deaths. However, because of insufcient medical facilities and inadequate data collection, JE cases are underreported. Thus, the true annual incidence of encephalitis cases is estimated to be closer to 175,000 (133). Recent outbreaks of JEV in northern India and Nepal between 2005 and 2007 have resulted in at least 11,000 cases and over 2000 deaths, highlighting the continued burden of disease in developing countries (93, 148). This review examines the ecology of JEV, details its emergence in new areas, and then assesses the potential for JEV to establish in the Americas, Europe, or Africa.
A multidisciplinary study on Honshu Island, Japan, demonstrated a basic cyclical pattern of JEV transmission between pigs, mosquitoes, and humans (58) (Figure 1). Typically, there are two suspected 4-day amplication cycles in pigs, with the initial cycle infecting approximately 20% of pigs, which usually develop antibodies by day 10 postinfection. Mosquitoes become infected by feeding on viremic pigs and, after a 7- to 14-day extrinsic incubation period (EIP), transmit the virus to other susceptible pigs. This second phase of viral amplication results in up to 100% porcine seroconversion. After another 714 days EIP in mosquitoes, human clinical cases begin to appear. Numerous other studies have demonstrated similar cycles of JEV transmission, although in some cases virus may be detected in mosquitoes prior to amplication in the pigs (28, 90). Differences in porcine infection rates within countries can also inuence human infection, as was evidenced in Sri Lanka, where porcine synchronous seroconversions led to signicant transmission to humans (91). However, no human cases were detected in areas where porcine asynchronous seroconversion occurred.
DISCOVERY OF AGENT AND ELUCIDATION OF TRANSMISSION CYCLE

JEV was originally isolated from the brain of a fatal human encephalitis case in Tokyo in 1934 (74) and from Culex tritaeniorhynchus mosquitoes in 1938 (73). Seminal experiments conducted near Tokyo in the 1950s elucidated the transmission cycle of JEV, with pigs and wild birds identied as amplifying hosts and Cx. tritaeniorhynchus incriminated as the primary vector species (summarized in Reference 6). Pigs are necessary for pre-epizootic amplication of the virus, although some epidemics do occur in the absence of high pig populations (119). Humans and horses can develop fatal encephalitis, but they are only incidentally infected and are dead-end hosts of the virus.
HUMAN INFECTION WITH JAPANESE ENCEPHALITIS VIRUS

Infection of humans with JEV produces a broad spectrum of clinical manifestations, ranging from asymptomatic infection, through mild febrile illness, to acute and lethal meningomyeloencephalitis (118). Most infections are asymptomatic or cause a nonspecic inuenza-like illness. Only 1 in 50 to 1 in 1000 infections result in encephalitic illness, although the reason why clinical disease is so rare is unknown (143). The ratio of symptomatic to asymptomatic cases has occasionally been higher [e.g., up to 1:25 in nonindigenous U.S. servicemen (34)]. The case fatality rate of JE can be as high as 67%, although between 20% and 40% is more typical, with children and the elderly at the greatest risk of fatal infection (33, 59, 89). Neurological sequelae occur in 45% to
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%
10 First outbreak 10 Second outbreak Third outbreak 100 80
% of pigs seroconverting to JEV
60 40 20
Pigs
4 Annu. Rev. Entomol. 2009.54:17-35. Downloaded from arjournals.annualreviews.org by 150.185.73.180 on 06/18/09. For personal use only. 14 4
Number of JEV isolations
Mosquitoes
14 4 14
Number of JE cases Humans

JUNE
Figure 1 Cyclic pattern of Japanese encephalitis virus transmission among pigs, mosquitoes, and humans (adapted from Reference 58).
10 5
JULY
AUGUST
SEPTEMBER
70% of survivors and can last for many years, with the remaining patients making a full recovery (21). Sequelae are more frequent in patients whose acute disease is severe, prolonged, and associated with coma and focal neurological decits (60).
GEOGRAPHICAL RANGE AND EPIDEMIOLOGICAL PATTERNS

JEV is distributed in temperate and tropical areas of eastern and southern Asia. Its geographic range extends from eastern Asia (China, Japan, Korea, maritime Siberia, Taiwan, the Philippines, and Vietnam), to Southeast Asia and northern Australasia (Cambodia, Indonesia, Laos, Malaysia, Papua New Guinea, Thailand, and the Torres Strait islands of northern Australia), and to southern Asia (Bangladesh, Bhutan, India, Myanmar, Nepal, and Sri Lanka) (10, 26, 70, 143) (Figure 2). A single
report has also suggested that JEV may occur in Pakistan (47). JE is largely a disease of rural areas, especially associated with irrigated rice agriculture. In general, two epidemiological patterns of JEV have been recognized: endemic activity in tropical regions, such as southern Thailand (11), and epidemic activity in temperate and subtropical regions, as rst described in Japan (59, 106). In endemic areas, no seasonal pattern exists and sporadic cases of encephalitis occur throughout the year, most often in infants and young children, although cases may peak after the onset of the rainy season. Serological tests have shown that by the time children reach adulthood all have been exposed to JEV and possess neutralizing antibodies. Epidemic activity in temperate and subtropical areas occurs most commonly in summer or early autumn after the rainy season, although this may extend from spring to late autumn, or even throughout
Neutralizing antibodies: antibodies induced during infection that bind to virus particles and inhibit infection of cells in vitro and in vivo
www.annualreviews.org Ecology and Geographical Expansion of JEV
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Figure 2 Geographical distribution of Japanese encephalitis virus based on current and historical data.
the year in more southern regions. Encephalitis cases in temperate areas are observed most often in children and young adults, although when epidemics occur in new areas or after long periods with no virus activity, all age groups may be affected (136). However, where childhood immunization has been included in the expanded program of immunization in temperate countries, such as Japan, South Korea, and Taiwan, JEV infections are becoming most common in the elderly. The two patterns of endemic and epidemic transmission tend to blur in subtropical regions such as northern Thailand and Vietnam, where epidemic activity may be super-
imposed on low-level endemic or year-round transmission.
Epidemics and the Evolution of JEV

Historically, epidemics of encephalitis attributable to JEV infection have been reported in Japan since 1871, but the rst well-described large outbreak occurred in Japan in 1924, with over 6000 cases and a fatality rate of 60%. Subsequent frequent summer epidemics suggested a seasonal occurrence and the possibility that transmission was through mosquito vectors. Summer epidemics were reported regularly
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every 23 years in Japan, Korea, and Taiwan until the mid-1960s, but no epidemics occurred thereafter owing to the introduction of childhood immunization programs and widespread use of pesticides on rice paddies. The records of the rst epidemics or isolations of JEV in other Asian countries have appeared to follow in a southeasterly direction (70, 116). Major epidemics were reported in northern Vietnam in 1965; in the Chiang Mai Valley of Thailand in 1969 and 1970 (33, 151); in West Bengal in 1973 (14); in the lowland (Terai) region of Nepal in 1978 (136); and in Sri Lanka in 198586 (144), with a larger epidemic in 1987 (90). Large outbreaks continue to occur in India, but the recent introduction of major immunization programs by state governments in collaboration with the Program for Appropriate Technology in Health (PATH) offers hope that epidemic activity may soon be controlled (17). Despite this apparent spread southward from Japan, molecular studies conversely suggest that JEV may have evolved in Southeast Asia and spread north (117). Studies of the geographic occurrence of JEV genotypes using nucleotide sequencing indicate that at least four, and possibly ve, genotypes of JEV can be distinguished. The only geographic area where all genotypes are found is the Indonesia-Malaysia region. Moreover, the oldest genotypes are also conned to this region.
ticorax nycticorax), plumed egret (Egretta intermedia), and little egret (Egretta garzetta), and all three species consistently displayed neutralizing and hemagglutination-inhibiting antibodies to JEV. Subsequent laboratory experiments demonstrated that postinoculation viremia was sufcient to infect Cx. tritaeniorhynchus (9, 32). Because of their close association with humans and varying levels of seroprevalence, pigeons, sparrows, ducks, and chickens have been implicated in natural transmission cycles of JEV, although their actual role in these cycles has not been clearly dened. Despite high seroprevalence rates in many mammal species (e.g., cattle, dogs, goats, and rodents), pigs are the only mammals that are important in the JEV transmission cycle. Pigs serve as amplifying hosts because they fulll the following criteria: (a) high natural infection rate (98%100%); (b) high viremia; (c) viremia that remains high enough to infect mosquitoes for up to 4 days; (d ) propensity for vector mosquitoes to feed on swine; and (e) high birth rate, providing a source of susceptible pigs every year (32, 108, 109). Although pigs are the major amplifying hosts of JEV, they can also act as maintenance hosts in endemic areas (53, 114). Although clinical disease is relatively rare, the primary illness associated with JEV infection in pigs is fetal abortion and stillbirth in infected sows and aspermia in boars (12, 129).
Enzootic: continuous virus amplication within an animal population Hemagglutinationinhibiting antibodies: antibodies induced during infection that bind to virus antigens and inhibit agglutination of erythrocytes in vitro
ECOLOGY OF JAPANESE ENCEPHALITIS VIRUS Vertebrate Hosts of JEV

Viremia and/or seroconversion to JEV has been observed in over 90 wild and domestic bird species belonging to a number of different avian families. However, ardeid wading birds are considered the primary enzootic hosts of JEV, and they can play a role in epizootic viral amplication in some areas (7, 101, 119). Field studies by Buescher and colleagues (7, 107) established the role of ardeids in the ecology of JEV. During a ve-year period, 54 strains of JEV were recovered from the black-crowned night heron (Nyc-
Vectors of JEV
Although JEV has been isolated from over 30 species, paddy-breeding mosquitoes of the Culex vishnui subgroup, particularly Cx. tritaeniorhynchus, are the major vectors of the virus. This is not surprising, as this species shares a similar ecological niche to Cx. tarsalis and Cx. annulirostris, the major vectors of JEV serological group viruses in the western United States and Australia, respectively (68, 95). A number of other species, such as Cx. gelidus, Cx. fuscocephala and Cx. annulirostris, have yielded numerous isolates, implicating them as important secondary or regional vectors (90, 99, 145).
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Mosquito infection rates display considerable geographical and temporal variation, reecting the complex interaction of climatic patterns, agricultural practices, mosquito population dynamics, and the presence of susceptible amplifying hosts. Infection rates can be as high as 1:233 or as low as 1:369,146, as have been observed in mosquitoes processed from Japan (8) and India (18), respectively. Distinctive seasonal patterns of virus activity in mosquitoes occur, with increases in infection rates linked to the warmer summer months in temperate areas (8) and the onset of the monsoon season in tropical areas (28). Laboratory experiments have conrmed the vector competence of Cx. tritaeniorhynchus for JEV. This species is susceptible to infection, with titers of only 12 log10 infectious units per mosquito required to infect some strains (126, 146). Subsequent transmission rates of 100% are commonly obtained and are a function of the virus titer of the initial blood meal and the temperature at which the mosquitoes are held. Other Culex spp. that are efcient laboratory vectors include Cx. pseudovishnui, Cx. gelidus, Cx. fuscocephala, Cx. annulirostris, and Cx. sitiens (25, 30, 79, 140). Cx. tritaeniorhynchus displays intraspecic variation in susceptibility to JEV infection, with Japanese strains generally more susceptible to infection than strains from Taiwan and Pakistan (127). The genetic basis for this difference in Cx. tritaeniorhynchus susceptibility has not been established. However, the discovery of multiple cytochrome oxidase I lineages of Cx. annulirostris may potentially explain differences in vector competence of these mosquitoes for JEV genotypes I and II in Australasia (40).
tion of the midgut, followed by high titer replication in the anterior section of the midgut. The second stage of multiplication occurred when the virus infected the fat body cells adjacent to the midgut, followed by infection of fat body cells in the hemocoel and, especially, between the thoracic muscles. The nal stage of multiplication occurred in the salivary glands and other susceptible organs including the compound eyes, thoracic ganglia, and Malpighian tubules. The EIP was temperature dependent and ranged from 6 days postinfection at 28 C to 20 days at 20 C (126). At low temperatures the transmission rate was reduced.
Host Feeding Patterns

An essential component of the JEV transmission cycle is the degree of contact between vectors and amplifying hosts. In classic host preference studies, cattle generally attracted more Cx. tritaeniorhynchus than pigs did (42, 81), reportedly a result of physiological conditioning rather than inherent genetic factors (80). Throughout their geographical range, most JEV vectors are opportunistic blood feeders, with host availability being the key factor inuencing host feeding patterns. High porcine feeding rates are generally reective of high pig populations and Cx. tritaeniorhynchus readily feeds on pigs when available (4, 92). Indeed, pig feeding rates of 30%40% have been recorded from South Korea (111) and northern India (5). However, throughout much of its geographical range, Cx. tritaeniorhynchus obtains most blood meals from cattle (16, 31, 75, 97), and because bovines do not produce sufcient viremia to infect mosquitoes, they may impede transmission of JEV and provide passive zooprophylaxis (48, 80). Humans account for only a small proportion (less than 5%) of blood meals for most Culex vectors of JEV in Asia.
Multiplication of JEV in Mosquitoes

A series of studies using uorescent antibody techniques was undertaken in the 1960s to determine the mode of development of JEV in infected Cx. tritaeniorhynchus, Cx. pipiens pallens, and Cx. quinquefasciatus (22, 24). Following ingestion of a viremic blood meal, JEV rapidly infected the epithelial cells of the posterior por22 van den Hurk
VIRUS SURVIVAL AND REINTRODUCTION

A variety of mechanisms may explain the ability of JEV to survive during interepidemic or
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interepizootic periods, adverse conditions associated with winter or dry season, or the period before the virus is reintroduced. Possible mechanisms include persistence in enzootic foci within vertebrate hosts and/or mosquitoes and reintroduction of the virus by migratory birds and/or mosquitoes.
Overwintering Mechanisms
The duration of viremia of JEV in birds and pigs is too short for these animals to effectively maintain the virus during adverse conditions. However, experimentally inoculated bats can sustain low levels of virus in the blood and brown adipose tissue during simulated hibernation at low temperatures; when the bats were returned to 24 C, virus multiplication was activated, raising viremia that invaded other tissues (123). Transplacental transmission in bats has also been demonstrated, which could enhance viral persistence (124). Experimentally infected lizards, snakes, and frogs also develop a viremia under simulated hibernation (23, 63, 87). However, these results are difcult to interpret because eld isolations from poikilothermic vertebrates have only been obtained during summer or autumn rather than spring, which would provide evidence for these animals maintaining the virus through the winter (102). Experimentally infected Cx. tritaeniorhynchus and Cx. quinquefasciatus transmit the virus to susceptible hosts following overwintering (44, 71). Despite this, JEV has only been isolated once from eld-collected overwintering Cx. tritaeniorhynchus, although only low numbers have ever been processed during the winter months (39). Importantly, the female Cx. tritaeniorhynchus rarely takes a blood meal prior to hibernation, thus reducing its exposure to viremic animals (86). In Korea, JEV has been isolated twice during winter from Cx. pipiens (63). Vertical transmission can facilitate overwintering of JEV when an infected female mosquito passes the virus to its progeny, which may then harbor the virus during adverse conditions dur-
ing the egg, larval, pupal, or adult stage. It appears that JEV, like other aviviruses, enters the fully formed egg through the micropyle at the time of fertilization just prior to oviposition, unlike true transovarial transmission (103). Laboratory transmission studies have demonstrated that vertical transmission occurs through the F1 generation of larvae and adults of numerous species, including Cx. tritaeniorhynchus, Cx. pipiens pallens, Cx. pipiens molestus, Cx. quinquefasciatus, Cx. vishnui, Aedes albopictus, Ae. alcasidi, Ae. japonicus, Ae. togoi, Ae. vexans, and Armigeres avus (104, 105, 128). However, these results are difcult to interpret in terms of natural transmission cycles, as parenteral inoculation was used as the mode of infection in many instances and JEV is rarely isolated from eldcollected immatures or adult male mosquitoes. Indeed, over a 3.5-year period in Taiwan, only one isolate of JEV was obtained from almost 400,000 Cx. tritaeniorhynchus larvae, compared with 164 isolates obtained from about 142,000 adult females (103). Additional eld isolates have been obtained from larvae or adult males of Cx. tritaeniorhynchus, Cx. pseudovishnui, Cx. pipiens pallens and Ae. albopictus (20, 43, 85).
Introduction by Migrating Birds, Bats, or Mosquitoes

Migratory birds or bats and/or wind-borne mosquitoes could reintroduce JEV into temperate regions (84, 117). Alternatively, wind-borne mosquitoes may periodically reintroduce the virus from endemic southern areas of Asia. Indeed, JEV transmission does not occur until after the onset of the southwest winds in temperate areas of Asia (112), and Cx. tritaeniorhynchus has been collected up to 500 km offshore in the Pacic Ocean (1) and at an altitude of over 380 m (72). Subsequent long-distance southern migration of Cx. tritaeniorhynchus before winter is also observed in northern latitudes during autumn, with a potential dispersal of 200 km per night (72). Finally, backtrack simulations indicated that northerly winds associated with tropical lows west of Cape York Peninsula could have transported mosquitoes from the
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island of New Guinea to northern Australia in 1998 (100).
PREVENTION AND CONTROL OF JEV

The prevention and control of JEV transmission can be achieved by three possible strategies, each targeting a specic part of the transmission cycle: (a) vaccination of the human population, (b) control of amplifying hosts by either swine vaccination or changes in animal husbandry, or (c) vector control. Human vaccination is considered the most reliable method of preventing JE in humans.
Vaccination
Until recently, the only vaccine available internationally and recommended for travelers was the mouse brain-derived, formalin-inactivated vaccine developed using the prototype Nakayama strain, which was manufactured and exported by the Biken Institute in Japan (113). Similar vaccines were manufactured in China, Japan, Korea, Taiwan, India, Thailand, and Vietnam (27). Use of this vaccine has almost eliminated the incidence of disease in Japan, Korea, and Taiwan (46, 115, 150), although other activities such as vector control and alternative agricultural practices have all contributed to the reduction in disease (46). Inactivated cell culture vaccines prepared in primary hamster kidney (PHK) or African green monkey kidney (Vero) cells, and a live attenuated SA14-14-2 vaccine have been used in China (64). The SA14-14-2 vaccine has also been used successfully in Nepal (130), and most recently in India (3). The latter recorded some adverse events, although the WHO Global Advisory Committee on Vaccine Safety (WHOGACVS) concluded that no serious adverse events related to the vaccine had occurred; however, they recommended that improved monitoring should be undertaken (149). There has been a long-held perception of signicant risk in using the inactivated mouse brain-derived Biken vaccine, particu24 van den Hurk
larly with regard to neurological and allergic reactions (125). Indeed, the Japanese government stopped recommending its use following a single case of acute disseminated encephalomyelitis after vaccination. However, as the link between the vaccine and this severe reaction could not be denitively proven, the WHOGACVS concluded that there was no reason to change current immunization recommendations (147). Despite this, manufacture of the Biken vaccine was discontinued in 2005, necessitating the development of suitable replacement vaccines. Currently, a number of vaccines are under development or in clinical trial for international use (3). These include the inactivated Vero-cell-derived SA14-14-2 vaccines (66, 121) and a live attenuated chimeric vaccine based on the ChimeriVax infectious clone of 17D yellow fever vaccine containing the prM and E genes of SA14-14-2 virus (78). These vaccines, together with the potential licensing of the SA14-14-2 attenuated vaccine in the future, suggest that replacements for the discontinued Biken vaccine will soon be available.
Control Measures Targeting Vertebrate Hosts

Some protection against swine abortion is afforded by vaccination of sows (56). However, swine vaccination is not effective or practical for preventing transmission to humans. Because most pigs are slaughtered at 68 months of age, annual vaccination of newborn piglets is required and maternal antibodies render the liveattenuated vaccine ineffective against pigs less than 6 months of age (46). The reduction of JE incidence in Japan, Taiwan, and Korea has been partially linked to the relocation of domestic pigs to specialized farms sited away from human habitation (120, 136, 150). Finally, in Japan, vaccination of horses has been carried out during the JEV transmission season each year since 1948 (82), resulting in a decrease in incidence of equine encephalitis (29). Indeed, vaccination of race horses is mandatory in several countries, including Singapore, Malaysia, and Hong Kong.
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Mosquito Control
Although ultralow-volume insecticide application has had some success in Southeast Asia (110), it is generally accepted that such vector control is impractical and costly during large, widespread outbreaks (10, 45, 133, 143). The extensive rice paddies that provide larval habitats for Cx. vishnui subgroup mosquitoes, coupled with the isolation of rural villages, make it virtually impossible to employ large-scale chemical treatment to control JEV transmission (62). However, the widespread application of pesticides to control agricultural insects has had the added benet of also reducing mosquito populations (61, 76, 150). Indoor residual spraying using DDT and other chemicals to control malaria is largely ineffective in reducing JEV transmission, owing to the largely exophilic resting behavior of the vector mosquitoes, although JE incidence was reduced in China, where pyrethroid-impregnated bed nets were deployed (65). In most JEV endemic rural settings, where vaccination rates are often low, an integrated vector management approach incorporating alternating wet and dry irrigation and larvivorous sh can reduce vector populations and potentially JEV transmission (54, 62).
spread the virus regionally (70). Viremic migratory birds (84) and even bats, especially fruit bats (Megachiroptera) (2, 122), may be involved in distant transport. Wind-blown infected mosquitoes have been suggested for the dispersal of JEV in China (72) and into Australia (100). The incidental transport of infected mosquitoes on aircraft has been implicated (38), and it has been suggested that Japanese troop movements in World War II may have introduced JEV into areas of Southeast Asia, possibly via transport of infected mosquitoes in aircraft or equipment, or via infected pigs (70). Rice irrigation and fertilizers that have resulted in increased vector populations, and increased pig production, have all been associated with the spread and establishment of JEV in new areas (54, 70, 132).
Culex sitiens subgroup: a group of morphologically similar species within the subgenus Culex (Culex), from which Cx. annulirostris is the primary Australasian JEV vector
The Australian Experience

While JEV has recently appeared in Australia, it is noteworthy that after more than 10 years, the virus has apparently not become established on the mainland, let alone spread beyond the region. This is despite predictions that when JEV rst appeared in a widespread outbreak on the Torres Strait islands in 1995 (37), it was feared that it would spread to the mainlands Cape York Peninsula, where populations of feral pigs, wading birds, and mosquitoes were prolic (67). In light of the explosive spread of WNV in the Americas, the apparent inability of JEV to establish warrants a detailed discussion. When compared to the Torres Strait islands, where intense activity has resulted in repeated mosquito isolates and widespread rapid seroconversion of pigs, recorded JEV transmission has been of a low level on Cape York Peninsula. First, fewer domestic pigs are housed in Cape York Peninsula communities and seroconversion of these pigs to JEV during two incursions of JEV into Cape York Peninsula in 1998 and 2004 has been asynchronous, thus limiting the pool of available epizootic hosts (36). Second, collections of 48,495 Culex sitiens subgroup mosquitoes on Cape York Peninsula in 1998 and 2004 yielded only one JEV isolate
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THE SPREAD OF JAPANESE ENCEPHALITIS VIRUS

In common with other members of the JEV serological complex, JEV has shown a propensity to spread and establish in new areas, most recently in the eastern Indonesian archipelago, the island of New Guinea, the Torres Strait of northern Australia (68), and southwest India (96). The incidence and spread of JEV has recently been extensively reviewed by Mackenzie et al. (70).
Mechanisms of JEV Movement

Several mechanisms could explain the spread of JEV. Natural cycling involving mosquitoes, pigs, and ardeid birds is thought to have
(in 2004) (138, 139), whereas comparable collections during JEV outbreaks on Badu Island in the Torres Strait yielded 66 JEV isolates (51, 99, 141). Finally, with the exception of a single human clinical case, there is no serological evidence of human JEV infections on Cape York Peninsula from serosurveys of 1092 individuals in seven communities following the 1998 outbreak (36). Furthermore, no JEV activity has been detected in mainland sentinel pigs in years following the Cape York Peninsula incursions (139). Although it is possible that some JEV transmission is cryptically maintained in foci on Cape York Peninsula, JEV certainly has not become a signicant public health issue on the Australian mainland. Several mechanisms have been proposed to account for the failure for JEV to become established on the Australian mainland. Cape York Peninsula has several endemic aviviruses, such as KUNV, MVEV, and Kokobera virus (50, 138), that might cross-protect pigs from infection with JEV (36). However, JEV cocirculates with related aviviruses in Papua New Guinea (52) and India (101). Different lineages of Cx. annulirostris occur on Cape York Peninsula and southern Papua New Guinea and may differ in their vector competence for JEV. Indeed, there is preliminary evidence to suggest that the most widely distributed mainland Australian lineage of Cx. annulirostris is a relatively inefcient laboratory vector of genotype I JEV that has been circulating in northern Australia since 2000 (40). The presence of alternative hosts may serve to minimize blood feeding by Cx. sitiens subgroup mosquitoes on feral pigs. Analysis of host feeding patterns revealed that only 5% and 1% of bloodfed Cx. sitiens subgroup mosquitoes collected from rural locations on western Cape York Peninsula had fed on birds and pigs, respectively (137). Most (75%) of these blood meals were of marsupial origin and were retrospectively identied to be from the agile wallaby (Macropus agilis) (142), which is abundant on Cape York Peninsula but absent from most Torres Strait islands. When experimentally inoculated with JEV, both Tammar walla26 van den Hurk
bies (Macropus eugenii) and agile wallabies failed to develop a viremia (69). Indeed, if agile wallabies are an unsuitable JEV host, then preferential blood feeding by Culex on this species could effectively dampen transmission and prevent virus maintenance (137). The only areas on Cape York Peninsula where JEV has been detected in pigs or mosquitoes had local concentrations of domestic or feral pigs, accompanied by a high incidence of blood feeding by Cx. sitiens subgroup mosquitoes on pigs (137, 139).
POTENTIAL EMERGENCE AND PUBLIC HEALTH RISK TO REGIONS OUTSIDE ITS NATURAL RANGE
Considering its propensity to spread, JEV could become established in new ecosystems outside of its current range. However, unlike the recent expansion into India and Australasia, where overlapping natural cycles are thought to have introduced the virus, JEV would have to traverse great distances over the Pacic Ocean, the Indian Ocean, and the deserts and mountains to the northwest of Pakistan to infest the Americas, Europe, or Africa. Introduction by migratory birds is plausible, although the migration routes of ardeid birds are generally north-south rather than east-west, and birds would no longer be viremic after the long journey from Asia. Instead, human-transported mosquitoes or viremic vertebrates would be more likely mechanisms, as has been proposed for the potential introduction of WNV into Hawaii from the United States (55). However, owing to animal quarantine procedures and the short duration of viremia in birds and pigs, the most likely mechanism of introduction would be via an infected mosquito transported by aircraft from a JEV endemic area. Indeed, high populations of adult Cx. tritaeniorhynchus occur near Narita International Airport, Japan, and this species has been collected in aircraft originating from other locations in Asia (38). Should JEV be introduced into a new region, a range of factors will inuence its establishment, as illustrated using a hypothetical
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North American scenario. The areas at potentially greatest risk are those with intensive pig rearing, such as the Midwestern United States, where swine populations exceed 30 million head (83). However, many of these are reared within purpose-built buildings and may not be exposed to signicant mosquito feeding, and the Australian experience suggests that JEV may be unable to establish itself in areas if vectors cannot or do not access signicant swine populations. For it to establish, JEV may have to exploit native or introduced vertebrate species in much the same way as WNV, for which endemic birds (57), reptiles (49), and mammals (88) have been implicated in transmission cycles. Numerous species of ardeid wading birds occur in North America, including widespread resident populations of N. nycticorax and the cattle egret (Bubulcus ibis), two species involved in JEV transmission in Asia (98). Other bird species common to both Asia and North America, including English sparrows, house nches, pigeons, ducks, and chickens, produce viremia after experimental infection (15, 19, 35). However, these bird species do not contribute to epidemic JEV transmission to the same extent as ardeid birds and pigs, possibly because they only produce a low-level viremia, and Cx. tritaeniorhynchus rarely feeds on them. Nonetheless, there are guilds of ornithophilic Culex species (77) that may facilitate enzootic transmission through these birds in North America. Should common urban fauna act as vertebrate hosts, JEV could become established in both urban and rural locations. Prior infection of vertebrate hosts with endemic aviviruses, such as SLEV and WNV, may provide some level of immunity against JEV, thus reducing the pool of available hosts to facilitate enzootic transmission. However, the cocirculation of JEV and MVEV in Papua New Guinea, and of JEV and WNV in Pakistan, suggest that sufcient populations of susceptible hosts exist to allow concurrent circulation of these closely related aviviruses in the same ecosystem (52, 101).
A number of secondary or moderately susceptible JEV vectors already occur in North America, including Cx. pipiens, Cx. quinquefasciatus, Ae. albopictus, Ae. japonicus, and Ae. vexans. However, endemic Culex spp. are more likely to be involved in local transmission, especially vectors of endemic JEV serological group aviviruses, such as Cx. tarsalis, Cx. pipiens, Cx. salinarius, and Cx. nigripalpis. Vector competence experiments with North American mosquitoes conducted in the 1940s not only conrmed that Cx. tarsalis and Cx. pipiens could serve as laboratory vectors of JEV but also incriminated nonCulex species, including Ae. dorsalis and Culiseta inornata (94). The introduction and establishment of JEV in a virgin ecosystem, such as the United States, could have dramatic consequences for human and animal health. JEV has a higher rate of severe neurological disease compared with other endemic encephalitic aviviruses, such as SLEV and WNV (134, 135). Additionally, SLEV and WNV more often cause severe disease in the elderly, whereas both children under 5 years of age and the elderly typically develop severe clinical manifestations following JEV infection. Furthermore, when JEV emerges in an immunologically na ve population, clinical disease occurs in all age groups (13, 41). Finally, in terms of animal disease, signicant equine morbidity and mortality could occur, and severe disease may develop in previously unexposed vertebrate species, as has occurred with WNV infection in birds (57) and alligators (49). A comprehensive contingency plan is necessary to limit the potential impact of JEV should it emerge in a region outside of its current geographical distribution. This plan should include an active surveillance system, comprising human and animal clinical case diagnosis, coupled with JEV-specic diagnostic assays for rapid detection of an incursion. Should the virus become established, control programs will have to be implemented, potentially at signicant economic cost to all levels of government. Widespread immunization of residents at risk
27
may be needed, with introduction of the vaccine into the early childhood vaccination schedule. Tourism could be affected, especially if vaccination is recommended for travelers visiting endemic areas, as is the case with visitors to Southeast Asia (113). The economic impact on agriculture would also be considerable, as there would be concerns regarding the export of live-
stock and associated products, resulting in a requirement for widespread testing to verify freedom from infection. Importantly, the potential role that endemic mosquitoes and vertebrate species could play in transmission cycles needs to be assessed using laboratory-based infection and transmission experiments before an outbreak occurs.
SUMMARY POINTS 1. JEV is distributed throughout Southeast Asia and the Indian subcontinent, through the Indonesian archipelago, and into the Australasian zoogeographical region. 2. Recent outbreaks in northern India and Nepal have resulted in almost 11,000 cases and 2000 deaths. 3. JEV is maintained in an enzootic cycle between ardeid wading birds and Culex mosquitoes; pigs are important for epizootic transmission. 4. Although humans and horses develop fatal encephalitis, they are dead-end hosts. 5. Proposed overwintering mechanisms include persistence in vertebrates and/or mosquitoes and vertical transmission in the mosquito. Alternatively, migrating birds and/or bats and wind-assisted dispersal of mosquitoes may reintroduce the virus. 6. Control measures include human vaccination and, to a limited extent, alternative pig husbandry and vector control. 7. While JEV has expanded its range into northern Australia, it does not appear to have become established in natural transmission cycles. Possible reasons for this include (a) the presence of related aviviruses that may provide cross-protection against JEV infection in susceptible hosts; (b) different lineages of Cx. annulirostris, which may vary in their vector competence to the different genotypes of JEV; and (c) a propensity for Cx. annulirostris to feed on marsupials and not pigs or wading birds (experimentally infected marsupials, especially wallabies, do not produce high levels of viremia). 8. There is the potential for JEV to spread to the Americas, Europe, or Africa, but the long distance from endemic areas makes this difcult, and modern pig husbandry may impede virus amplication.
FUTURE ISSUES 1. Modeling should be used to investigate why JEV has failed to establish in mainland Australia, as well as its potential for spread and establishment in North America, Europe, and Africa. 2. Assessment is needed whether JEV could establish in a new region by conducting vector competence experiments with native mosquito species, especially those belonging to the genus Culex. In addition, conducting laboratory-based infection studies of common
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vertebrate fauna with JEV may determine their potential role in JEV transmission cycles. This will provide information to facilitate a targeted response should the virus be introduced. 3. The genetic basis for the variation in vector competence between populations of Cx. tritaeniorhynchus and other vector species should be investigated. 4. Culex ecology, especially blood-feeding behavior, near modern intensive pig-rearing facilities or ardeid roosts should be investigated. 5. It should be assessed whether infection of vertebrates with endemic aviviruses, including MVEV, WNV and SLEV, provides cross-protection or immune enhancement following infection with JEV.
6. More specic serological assays are required to differentiate JEV from related aviviruses. 7. Development and adoption of safe, low-cost, and effective vaccine candidates is needed.
DISCLOSURE STATEMENT
The authors are not aware of any biases that might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
We wish to acknowledge the invaluable contribution of Laila Whiteing of Queensland Health and Tony Sweeney for preparation of the gures, and Richard Russell, Roy Hall, Cassie Jansen, and Jay Nicholson for reviewing a draft of the manuscript. We also thank Marc Klowden and Dan Kline during the genesis of ideas presented in this review. LITERATURE CITED
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www.annualreviews.org Ecology and Geographical Expansion of JEV 33
117. Suggests that the different JEV genotypes evolved from an ancestral virus in Indonesia-Malaysia and spread across Asia.
126. Details the intrinsic and extrinsic factors that inuence the vector competence of Cx. tritaeniorhynchus for JEV.
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130. Tandan JB, Ohrr H, Sohn YM, Yoksan S, Ji M, et al. 2007. Single dose of SA 14-14-2 vaccine provides long-term protection against Japanese encephalitis: a case-control study in Nepalese children 5 years after immunization. Vaccine 25:504145 131. Thiel H-J, Collett MS, Gould EA, Heinz FX, Houghton M, et al. 2005. Flaviviridae. In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses, ed. CM Fauquet, MA Mayo, J Maniloff, U Desselberger, LA Ball, pp. 98198. San Diego: Virol. Div., Int. Union Microbiol. Soc. 132. Tsai TF. 1997. Factors in the changing epidemiology of Japanese encephalitis and West Nile fever. In Factors in the Emergence of Arbovirus Diseases, ed. JF Saluzzo, B Dodet, pp. 17989. Paris: Elsevier 133. Tsai TF. 2000. New initiatives for the control of Japanese encephalitis by vaccination: minutes of a WHO/CVI meeting, Bangkok, Thailand, 1315 Oct. 1998. Vaccine 18:125 134. Tsai TF, Mitchell CJ. 1989. St. Louis encephalitis. In The Arboviruses: Epidemiology and Ecology, ed. TP Monath, pp. 11343. Boca Raton, FL: CRC Press 135. Tyler KL. 2004. West Nile virus infection in the United States. Arch. Neurol. 61:119095 136. Umenai T, Krzysko R, Bektimirov TA, Assaad FA. 1985. Japanese encephalitis: current worldwide status. Bull. WHO 63:62531 137. van den Hurk AF, Johansen CA, Zborowski P, Paru R, Foley PN, et al. 2003. Mosquito host-feeding patterns and implications for Japanese encephalitis virus transmission in northern Australia and Papua New Guinea. Med. Vet. Entomol. 17:40311 138. van den Hurk AF, Johansen CA, Zborowski P, Phillips DA, Pyke AT, et al. 2001. Flaviviruses isolated from mosquitoes collected during the rst outbreak of Japanese encephalitis virus on Cape York Peninsula, Australia. Am. J. Trop. Med. Hyg. 64:12530 139. van den Hurk AF, Montgomery BL, Northill JA, Smith IL, Zborowski P, et al. 2006. The rst isolation of Japanese encephalitis virus from mosquitoes collected from mainland Australia. Am. J. Trop. Med. Hyg. 75:2125 140. van den Hurk AF, Nisbet DJ, Hall RA, Kay BH, Mackenzie JS, Ritchie SA. 2003. Vector competence of Australian mosquitoes (Diptera: Culicidae) for Japanese encephalitis virus. J. Med. Entomol. 40:8290 141. van den Hurk AF, Ritchie SA, Smith GA, Montgomery BL, Mackenzie JS. 2005. A Japanese encephalitis odyssey: entomological studies in northern Australia, 20022004. Arbovirus Res. Aust. 9:37077 142. van den Hurk AF, Smith IL, Smith GA. 2007. Development and evaluation of real-time polymerase chain reaction assays to identify mosquito (Diptera: Culicidae) blood meals originating from native Australian mammals. J. Med. Entomol. 44:8592 143. Vaughn DW, Hoke CH. 1992. The epidemiology of Japanese encephalitis: prospects for prevention. Epidemiol. Rev. 14:197221 144. Vitarana T, Jayasekera N, Wedasinghe N, Senaratne A, Colombage G, et al. 1988. The 1985/86 Japanese encephalitis outbreak in Sri Lanka and the impact of new irrigation schemes. In Virus Diseases in Asia, ed. P Thongcharoen, E Kurstak, pp. 19396. Bangkok: Mahidol Univ. 145. Vythilingam I, Oda K, Mahadevan S, Abdullah G, Thim CS, et al. 1997. Abundance, parity, and Japanese encephalitis virus infection of mosquitoes (Diptera: Culicidae) in Sepang District, Malaysia. J. Med. Entomol. 34:25762 146. Weng MH, Lien JC, Lin CC, Yao CW. 2000. Vector competence of Culex pipiens molestus (Diptera: Culicidae) from Taiwan for a sympatric strain of Japanese encephalitis virus. J. Med. Entomol. 37:78083 147. WHO. 2005. WHO Global Advisory Committee on Vaccine Safety, 910 June. Wkly. Epidemiol. Rec. 80:24247 148. WHO. 2006. Immunization and Vaccine Development. Japanese Encephalitis. Geneva: WHO 149. WHO. 2006. WHO Global Advisory Committee on Vaccine Safety, 2930 Nov. Wkly. Epidemiol. Rec. 82:1824 150. Wu YC, Huang YS, Chien LJ, Lin TL, Yueh YY, et al. 1999. The epidemiology of Japanese encephalitis on Taiwan during 19661997. Am. J. Trop. Med. Hyg. 61:7884 151. Yamada T, Rojanasuphot S, Takagi M, Wungkobkiat S, Hirota T, et al. 1971. Studies on an epidemic of Japanese encephalitis in the northern region of Thailand in 1969 and 1970. Biken J. 14:26796
133. Addresses the true burden of disease due to JEV and summarizes different vaccination strategies employed in different countries.
35
Contents
Frontispiece Edward S. Ross p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p xiv Lifelong Safari: The Story of a 93-Year-Old Peripatetic Insect Hunter Edward S. Ross p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1 Ecology and Geographical Expansion of Japanese Encephalitis Virus Andrew F. van den Hurk, Scott A. Ritchie, and John S. Mackenzie p p p p p p p p p p p p p p p p p p p p p p p 17 Species Interactions Among Larval Mosquitoes: Context Dependence Across Habitat Gradients Steven A. Juliano p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 37 Role of Glucosinolates in Insect-Plant Relationships and Multitrophic Interactions Richard J. Hopkins, Nicole M. van Dam, and Joop J.A. van Loon p p p p p p p p p p p p p p p p p p p p p p p p 57 Conict, Convergent Evolution, and the Relative Importance of Immature and Adult Characters in Endopterygote Phylogenetics Rudolf Meier and Gwynne Shimin Lim p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 85 Gonadal Ecdysteroidogenesis in Arthropoda: Occurrence and Regulation Mark R. Brown, Douglas H. Sieglaff, and Huw H. Rees p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 105 Roles of Thermal Adaptation and Chemical Ecology in Liriomyza Distribution and Control Le Kang, Bing Chen, Jia-Ning Wei, and Tong-Xian Liu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 127 Fitness Costs of Insect Resistance to Bacillus thuringiensis Aaron J. Gassmann, Yves Carrire, and Bruce E. Tabashnik p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 147 Insect Herbivore Nutrient Regulation Spencer T. Behmer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 165 Manipulation of Host Behavior by Parasitic Insects and Insect Parasites Frederic Libersat, Antonia Delago, and Ram Gal p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 189 Bionomics of Bagworms (Lepidoptera: Psychidae) Marc Rhainds, Donald R. Davis, and Peter W. Price p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 209
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Host-Parasitoid Associations in Strepsiptera Jeyaraney Kathirithamby p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 227 Biology of the Parasitoid Melittobia (Hymenoptera: Eulophidae) Robert W. Matthews, Jorge M. Gonzlez, Janice R. Matthews, and Leif D. Deyrup p p p 251 Insect Pests of Tea and Their Management Lakshmi K. Hazarika, Mantu Bhuyan, and Budhindra N. Hazarika p p p p p p p p p p p p p p p p p p 267 New Insights into Peritrophic Matrix Synthesis, Architecture, and Function Dwayne Hegedus, Martin Erlandson, Cedric Gillott, and Umut Toprak p p p p p p p p p p p p p p p p 285
Adaptation and Invasiveness of Western Corn Rootworm: Intensifying Research on a Worsening Pest Michael E. Gray, Thomas W. Sappington, Nicholas J. Miller, Joachim Moeser, and Martin O. Bohn p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 303 Impacts of Plant Symbiotic Fungi on Insect Herbivores: Mutualism in a Multitrophic Context Sue E. Hartley and Alan C. Gange p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 323 A Study in Inspiration: Charles Henry Turner (18671923) and the Investigation of Insect Behavior Charles I. Abramson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 343 Monogamy and the Battle of the Sexes D.J. Hosken, P. Stockley, T. Tregenza, and N. Wedell p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 361 Biology of Subterranean Termites: Insights from Molecular Studies of Reticulitermes and Coptotermes Edward L. Vargo and Claudia Husseneder p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 379 Genetic, Individual, and Group Facilitation of Disease Resistance in Insect Societies Noah Wilson-Rich, Marla Spivak, Nina H. Fefferman, and Philip T. Starks p p p p p p p p p p 405 Floral Isolation, Specialized Pollination, and Pollinator Behavior in Orchids Florian P. Schiestl and Philipp M. Schlter p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 425 Cellular and Molecular Aspects of Rhabdovirus Interactions with Insect and Plant Hosts El-Desouky Ammar, Chi-Wei Tsai, Anna E. Whiteld, Margaret G. Redinbaugh, and Saskia A. Hogenhout p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 447 Role of Vector Control in the Global Program to Eliminate Lymphatic Filariasis Moses J. Bockarie, Erling M. Pedersen, Graham B. White, and Edwin Michael p p p p p p p 469
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ANNUAL REVIEWS

Ecology and Geographical Expansion of Japanese Encephalitis Virus

DISCOVERY OF AGENT AND ELUCIDATION OF TRANSMISSION CYCLE

HUMAN INFECTION WITH JAPANESE ENCEPHALITIS VIRUS

van den Hurk

% of pigs seroconverting to JEV

Number of JEV isolations

Number of JE cases Humans

GEOGRAPHICAL RANGE AND EPIDEMIOLOGICAL PATTERNS

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imposed on low-level endemic or year-round transmission.

Epidemics and the Evolution of JEV

van den Hurk

ECOLOGY OF JAPANESE ENCEPHALITIS VIRUS Vertebrate Hosts of JEV

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Host Feeding Patterns

Multiplication of JEV in Mosquitoes

VIRUS SURVIVAL AND REINTRODUCTION

Introduction by Migrating Birds, Bats, or Mosquitoes

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island of New Guinea to northern Australia in 1998 (100).

PREVENTION AND CONTROL OF JEV

Control Measures Targeting Vertebrate Hosts

The Australian Experience

THE SPREAD OF JAPANESE ENCEPHALITIS VIRUS

Mechanisms of JEV Movement

www.annualreviews.org Ecology and Geographical Expansion of JEV

www.annualreviews.org Ecology and Geographical Expansion of JEV

van den Hurk

70. A comprehensive review of JEV epidemiology.

www.annualreviews.org Ecology and Geographical Expansion of JEV

Annual Review of Entomology Volume 54, 2009

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