Ecology and Geographical Expension of JE

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Ecology and GeographicalExpansion of JapaneseEncephalitis Virus

Andrew F. van den Hurk,1,2 Scott A. Ritchie,3,4

and John S. Mackenzie5

1Virology, Queensland Health Forensic and Scientific Services, Archerfield, Queensland4108, Australia; email: andrew [email protected]

2School of Molecular and Microbial Sciences, The University of Queensland, St. Lucia,Queensland 4072, Australia

3Tropical Population Health Unit Network, Queensland Health, Cairns, Queensland 487Australia; email: scott [email protected]

4School of Public Health and Tropical Medicine, James Cook University, Cairns,Queensland 4870, Australia

5Australian Biosecurity Cooperative Research Center for Emerging Infectious Disease,Division of Health Sciences, Curtin University of Technology, GPO U1987, Perth,

Western Australia 6845, Australia, email: [email protected]

Annu. Rev. Entomol. 2009. 54:1735

The Annual Review of Entomology is online atento.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

flavivirus, Culex, pigs, wading birds, Asia

Abstract

Japanese encephalitis virus ( JEV) (Flavivirus: Flaviviridae) is a leadin

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, anCx. annulirostrisare important secondary or regional vectors. Contro

of JEV is achieved through human and/or swine vaccination, changes inanimal husbandry, mosquito control, or a combination of these strate

gies. 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 thUnited States as a case study.

17


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JEV: Japaneseencephalitis virus

JE: Japaneseencephalitis; refers tothe clinical disease inhumans

MVEV: MurrayValley encephalitisvirus

SLEV: St. Louisencephalitis virus

WNV: West Nilevirus

KUNV: Kunjin virus

Epizootic: a period ofincreased virusamplification within an

animal population,which can lead toincidental transmissionto humans

Extrinsic incubationperiod (EIP): thetime betweeningestion of the virusby the arthropodvector andtransmission during asubsequent blood meal

Synchronousseroconversion:where the majority ofpigs seroconvert in ashort period of time

Asynchronousseroconversion:where seroconversionis protracted, andsome animals do notdisplay antibodies evenby the end of thetransmission period

INTRODUCTION

Japanese encephalitis virus ( JEV) is a member

of the JEV serological complex, the membersof which cause significant morbidity and mor-

tality. The complex consists of eight speciesand 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 incidenceof 45,000humancasesand10,000 deaths. How-

ever, because of insufficient medical facilitiesand inadequate data collection, JE cases are un-

derreported. Thus, the true annual incidenceof encephalitis cases is estimated to be closer

to 175,000 (133). Recent outbreaks of JEV in

northern India and Nepal between 2005 and2007 have resulted in at least 11,000 cases andover 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 as-

sesses the potential for JEV to establish in theAmericas, Europe, or Africa.

DISCOVERY OF AGENT

AND ELUCIDATION OFTRANSMISSION CYCLE

JEV was originally isolated from the brain

of a fatal human encephalitis case in Tokyoin 1934 (74) and from Culex tritaeniorhynchus

mosquitoes in 1938 (73). Seminal experimentsconducted near Tokyo in the 1950s elucidated

thetransmissioncycle of JEV, with pigs andwildbirds identified as amplifying hosts and Cx. tri-

taeniorhynchusincriminated as the primary vec-tor species (summarized in Reference 6). Pigs

are necessary for pre-epizootic amplification ofthe virus, although some epidemics do occur in

the absence of high pig populations (119). Hu-

mans and horses can develop fatal encephalitis,but they are only incidentally infected and are

dead-end hosts of the virus.

A multidisciplinary study on Honshu IslaJapan, demonstrated a basic cyclical pattern

JEV transmission between pigs, mosquitoand humans (58) (Figure 1). Typically, th

are two suspected 4-day amplification cycles

pigs, with the initial cycle infecting appromately 20% of pigs, which usually develop an

bodies by day 10 postinfection. Mosquitoes come infected by feeding on viremic pigs a

after a 7- to 14-day extrinsic incubation per(EIP), transmit the virus to other suscepti

pigs. This second phase of viral amplificatresults in up to 100% porcine seroconversi

After another 714 days EIP in mosquitoes, hman clinical cases begin to appear. Numero

other studies have demonstrated similar cycof JEV transmission, although in some ca

virus may be detected in mosquitoes prior

amplification in the pigs (28, 90). Differenceporcine infection rates within countries can a

influence human infection, as was evidencedSri Lanka, where porcine synchronous se

conversions led to significant transmissionhumans (91). However, no human cases w

detected in areas where porcine asynchronoseroconversion occurred.

HUMAN INFECTION WITHJAPANESE ENCEPHALITIS VIRU

Infection of humans with JEV produce

broadspectrum of clinical manifestations, raning from asymptomatic infection, throu

mild febrile illness, to acute and letmeningomyeloencephalitis (118). Most inf

tions are asymptomatic or cause a nonspecinfluenza-like illness. Only 1 in 50 to 1

1000 infections result in encephalitic illness,though the reason why clinical disease is so r

is unknown (143). The ratio of symptomato asymptomatic cases has occasionally be

higher [e.g., up to 1:25 in nonindigenous U

servicemen (34)]. The case fatality rate ofcan be as high as 67%, although between 20

and 40% is more typical, with children and telderly at the greatest risk of fatal infection (

59, 89). Neurological sequelae occur in 45%

18 van den Hurk Ritchie Mackenzie


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JUNE JULY AUGUST SEPTEMBER

10

80

60

40

20

Pigs

10

4 4

4

14

14 14

First

outbreak

10

Second

outbreak

Third

outbreak

Mosquitoes

Humans

10

5

%

% of pigs

seroconverting

to JEV

Number of

JE cases

Number of

JEV isolations

Figure 1

Cyclic pattern of Japanese encephalitis virus transmission among pigs, mosquitoes, and humans (adapted from Reference 58).

70% of survivors and can last for many years,

with the remaining patients making a full re-covery (21). Sequelae are more frequent in pa-

tients whose acute disease is severe, prolonged,andassociated with coma andfocal neurological

deficits (60).

GEOGRAPHICAL RANGE ANDEPIDEMIOLOGICAL PATTERNS

JEV is distributed in temperate and tropical ar-

eas of eastern and southern Asia. Its geographic

range extends from eastern Asia (China, Japan,Korea, maritime Siberia, Taiwan, the Philip-

pines, and Vietnam), to Southeast Asia andnorthern 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

Neutralizing

antibodies:antibodies inducedduring infection thabind to virus particleand inhibit infectioncells in vitro andin vivo

report has also suggested that JEV may occur

in Pakistan (47).JE is largely a disease of rural areas, espe-

cially associated with irrigated rice agriculture.In general, two epidemiological patterns of

JEV have been recognized: endemic activityin tropical regions, such as southern Thailand

(11), and epidemic activity in temperate andsubtropical regions, as first described in Japan

(59, 106). In endemic areas, no seasonal patternexists and sporadic cases of encephalitis occur

throughout the year, most often in infants andyoung children, although cases may peak after

the onset of the rainy season. Serological tests

have shown that by the time children reachadulthood all have been exposed to JEV and

possess neutralizing antibodies. Epidemic ac-tivity in temperate and subtropical areas occurs

most commonly in summer or early autumnafter the rainy season, although this may extend

from spring to late autumn, or even throughout

www.annualreviews.org Ecology and Geographical Expansion of JEV 19


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Figure 2Geographical distribution of Japanese encephalitis virus based on current and historical data.

the year in more southern regions. Encephalitiscasesintemperateareasareobservedmostoften

in children and young adults, although when

epidemics occur in new areas or after long peri-ods with no virus activity, all age groups may be

affected (136). However, where childhood im-munization has been included in the expanded

program of immunization in temperate coun-tries, such as Japan, South Korea, and Taiwan,

JEV infections are becoming most common inthe elderly. The two patterns of endemic and

epidemic transmission tend to blur in subtrop-ical regions such as northern Thailand and

Vietnam,where epidemic activity may be super-

imposed on low-level endemic or year-routransmission.

Epidemics and the Evolution of JEV

Historically, epidemics of encephalitis tributable to JEV infection have been repor

in Japan since 1871, but the first well-describlarge outbreak occurred in Japan in 1924, w

over 6000 cases and a fatality rate of 60%. Susequent frequent summer epidemics sugges

a seasonal occurrence and the possibility thtransmission was through mosquito vecto

Summer epidemics were reported regula



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every 23 years in Japan, Korea, and Taiwanuntil the mid-1960s, but no epidemics occurred

thereafter owing to the introduction of child-hood immunization programs and widespread

use of pesticides on rice paddies. The records

of the first epidemics or isolations of JEV inotherAsiancountrieshaveappearedtofollowin

a southeasterly direction (70, 116). Major epi-demics were reported in northern Vietnam in

1965; in the Chiang Mai Valley of Thailand in1969and1970(33,151);inWestBengalin1973

(14); in the lowland (Terai) region of Nepal in1978 (136); and in Sri Lanka in 198586 (144),

with a larger epidemic in 1987 (90). Large out-breaks continue to occur in India, but the recent

introduction of major immunization programsby state governments in collaboration with the

Program for AppropriateTechnology in Health

(PATH) offers hope that epidemic activity maysoon be controlled (17).

Despite this apparent spread southwardfrom Japan, molecular studies conversely sug-

gest that JEV may have evolved in SoutheastAsia and spread north (117). Studies of the geo-

graphic occurrence of JEV genotypes using nu-cleotide sequencing indicate that at least four,

and possibly five, genotypes of JEV can be dis-tinguished. The only geographic area where all

genotypes are found is the Indonesia-Malaysiaregion. Moreover, the oldest genotypes are also

confined to this region.

ECOLOGY OF JAPANESEENCEPHALITIS VIRUS

Vertebrate Hosts of JEV

Viremia and/or seroconversion to JEV has beenobserved in over 90 wild and domestic bird

species belonging to a number of different avianfamilies. However, ardeid wading birds are con-

sidered the primary enzootic hosts of JEV, and

they can play a role in epizootic viral amplifica-tion in some areas (7, 101, 119). Field studies by

Buescher andcolleagues (7, 107) established therole of ardeids in the ecology of JEV. During a

five-year period, 54 strains of JEV were recov-ered from the black-crowned night heron (Nyc-

Enzootic: continuovirus amplificationwithin an animalpopulation

Hemagglutinationinhibiting antibodiantibodies inducedduring infection thabind to virus antigenand inhibitagglutination oferythrocytes in vitro

ticorax nycticorax), plumed egret (Egretta inter-media), and little egret (Egretta garzetta), and all

three species consistently displayed neutraliz-

ing and hemagglutination-inhibiting antibod-ies to JEV. Subsequent laboratory experiments

demonstrated that postinoculation viremia wassufficient to infectCx. tritaeniorhynchus(9, 32).

Because of their close association with humansand varying levels of seroprevalence, pigeons,

sparrows, ducks, and chickens have been im-plicated in natural transmission cycles of JEV,

although theiractual role in these cycles has notbeen clearly defined.

Despite high seroprevalence rates in manymammal species (e.g., cattle, dogs, goats, and

rodents), pigs are the only mammals that are

important in the JEV transmission cycle. Pigsserve as amplifying hosts because they fulfill

the following criteria: (a) high natural infectionrate (98%100%); (b) high viremia; (c) viremia

that remains high enough to infect mosquitoesfor up to 4 days; (d) propensity for vector

mosquitoes to feed on swine; and (e) high birthrate,providingasourceofsusceptiblepigsevery

year (32, 108, 109). Although pigs are the ma-jor 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 infectedsows and aspermia in boars (12, 129).

Vectors of JEV

Although JEV has been isolated from over

30 species, paddy-breeding mosquitoes of theCulex vishnuisubgroup, particularlyCx. tritae-

niorhynchus, are the major vectors of the virus.This is not surprising, as this species shares

a similar ecological niche to Cx. tarsalis andCx. annulirostris, the major vectors of JEV sero-

logical group viruses in the western United

States and Australia, respectively (68, 95). Anumber of other species, such as Cx. gelidus,Cx. fuscocephala and Cx. annulirostris, haveyielded numerous isolates, implicating them as

importantsecondary or regional vectors(90, 99,145).



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Mosquito infection rates display consid-erable geographical and temporal variation,

reflecting the complex interaction of climaticpatterns, agricultural practices, mosquito popu-

lation dynamics, andthepresence of susceptible

amplifying hosts. Infection rates can be as highas 1:233 or as low as 1:369,146, as have been

observed in mosquitoes processed from Japan(8) and India (18), respectively. Distinctive sea-

sonal patterns of virus activity in mosquitoesoccur, with increases in infection rates linked

to the warmer summer months in temperateareas (8) and the onset of the monsoon season

in tropical areas (28).Laboratory experiments have confirmed the

vector competence of Cx. tritaeniorhynchus forJEV. 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 ofthe virus titer of the initial blood meal and the

temperature at which the mosquitoes are held.Other Culex spp. that are efficient laboratory

vectors include Cx. pseudovishnui, Cx. gelidus,Cx. fuscocephala, Cx. annulirostris, and Cx. sitiens

(25, 30, 79, 140).Cx. tritaeniorhynchus displays intraspecific

variation in susceptibility to JEV infection, with

Japanese strains generally more susceptible toinfection than strains from Taiwan and Pakistan

(127). The genetic basis for this difference inCx. tritaeniorhynchussusceptibility has not been

established. However, the discovery of multi-ple cytochrome oxidase I lineages of Cx. an-

nulirostrismay potentially explain differences invector competence of these mosquitoes for JEV

genotypes I and II in Australasia (40).

Multiplication of JEV in Mosquitoes

A series of studies using fluorescent antibody

techniques was undertaken in the 1960s to de-termine the mode of development of JEV in

infected Cx. tritaeniorhynchus, Cx. pipiens pallens,

and Cx. quinquefasciatus(22, 24). Following in-

gestion of a viremic blood meal, JEV rapidlyinfected the epithelial cells of the posterior por-

tion of the midgut, followed by high titer repcation in the anterior section of the midg

The second stage of multiplication occurwhen the virus infected the fat body cells

jacent to the midgut, followed by infection

fat body cells in the hemocoel and, especiabetween the thoracic muscles. The final sta

of multiplication occurred in the salivary glanandothersusceptible organsincluding theco

pound eyes, thoracic ganglia, and Malpightubules. The EIP was temperature depend

and ranged from 6 days postinfection at 28to 20 days at 20C (126). At low temperatu

the transmission rate was reduced.

Host Feeding Patterns

An essential component of the JEV transm

sion cycle is the degree of contact between vtors and amplifying hosts. In classic host pr

erence studies, cattle generally attracted mCx. tritaeniorhynchusthan pigs did (42, 81),

portedly a result of physiological conditioing rather than inherent genetic factors (8

Throughout their geographical range, mJEV vectors are opportunistic blood feede

with host availability being the key factor fluencing host feeding patterns. High porc

feeding rates are generally reflective of h

pig populationsand Cx. tritaeniorhynchusreadfeeds on pigs when available (4, 92). Indeed,

feeding rates of 30%40% have been recordfrom South Korea (111) and northern India

However, throughout much of its geographirange, Cx. tritaeniorhynchusobtains most blo

meals from cattle (16, 31, 75, 97), and becabovines do not produce sufficient viremia

infect mosquitoes, they may impede transmsion of JEV and provide passive zooprophyla

(48, 80). Humans account for only a small pportion (less than 5%) of blood meals for m

Culex vectors of JEV in Asia.

VIRUS SURVIVAL ANDREINTRODUCTION

A variety of mechanisms may explain the abity of JEV to survive during interepidemic



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interepizootic periods, adverse conditions as-sociated with winter or dry season, or the pe-

riod before the virus is reintroduced. Possiblemechanismsinclude persistencein enzootic foci

within vertebrate hosts and/or mosquitoes and

reintroduction of the virus by migratory birdsand/or mosquitoes.

Overwintering Mechanisms

The duration of viremia of JEV in birds and

pigs is too short for these animals to effec-tively maintain the virus during adverse condi-

tions. However, experimentally inoculated batscan sustain low levels of virus in the blood and

brown adipose tissue during simulated hiber-

nation at low temperatures; when the bats werereturned to 24C, virus multiplication was acti-

vated, raising viremia that invaded other tissues(123). Transplacental transmission in bats has

also been demonstrated, which could enhanceviral persistence (124).

Experimentally infected lizards, snakes, andfrogs also develop a viremia under simulated

hibernation (23, 63, 87). However, these re-sults aredifficult to interpret because field isola-

tions from poikilothermic vertebrates have onlybeenobtained duringsummeror autumnrather

than spring, which would provide evidence for

these animals maintaining the virus through thewinter (102).

Experimentally infected Cx. tritae-

niorhynchus and Cx. quinquefasciatus trans-

mit the virus to susceptible hosts followingoverwintering (44, 71). Despite this, JEV has

only been isolated once from field-collectedoverwintering Cx. tritaeniorhynchus, although

only low numbers have ever been processedduring the winter months (39). Importantly,

the female Cx. tritaeniorhynchus rarely takes ablood meal prior to hibernation, thus reducing

its exposure to viremic animals (86). In Korea,

JEV has been isolated twice during winterfrom Cx. pipiens(63).

Vertical transmission can facilitate overwin-teringofJEVwhenaninfectedfemalemosquito

passes the virus to its progeny, which may thenharbor the virus during adverse conditions dur-

ing the egg, larval, pupal, or adult stage. It ap-pears that JEV, like other flaviviruses, enters the

fully formed egg through the micropyle at thetimeoffertilizationjustpriortooviposition,un-

like true transovarial transmission (103). Labo-ratory transmission studies have demonstrated

that vertical transmission occurs through the

F1

generation of larvae and adults of nu-merous species, including Cx. tritaeniorhynchus,

Cx. pipiens pallens, Cx. pipiens molestus, Cx. quin-quefasciatus, Cx. vishnui, Aedes albopictus, Ae. al-

casidi, Ae. japonicus, Ae. togoi, Ae. vexans, andArmigeres flavus(104, 105, 128). However, these

results are difficult to interpret in terms of nat-ural transmission cycles, as parenteral inocula-

tion was used as the mode of infection in manyinstances and JEV is rarely isolated from field-

collected immatures or adult male mosquitoes.

Indeed, over a 3.5-year period in Taiwan, onlyone isolate of JEV was obtained from al-

most 400,000 Cx. tritaeniorhynchuslarvae, com-pared with 164 isolates obtained from about

142,000 adult females (103). Additional fieldisolates have been obtained from larvae or adult

males ofCx. tritaeniorhynchus, Cx. pseudovishnui,Cx. pipiens pallensand Ae. albopictus(20, 43, 85).

Introduction by Migrating Birds,Bats, or Mosquitoes

Migratory birds or bats and/or wind-borne

mosquitoescouldreintroduceJEVintotemper-ate regions (84, 117). Alternatively, wind-borne

mosquitoes may periodically reintroduce thevirus from endemic southern areas of Asia. In-

deed, JEV transmission does not occur until af-ter the onset of the southwest winds in temper-

ate areas of Asia (112), and Cx. tritaeniorhynchushas been collected up to 500 km offshore in

the Pacific Ocean (1) and at an altitude of over380 m (72). Subsequent long-distance southern

migration of Cx. tritaeniorhynchus before win-

ter is also observed in northern latitudes duringautumn, with a potential dispersal of 200 km

per night (72). Finally, backtrack simulationsindicated that northerly winds associated with

tropical lows west of Cape York Peninsulacould have transported mosquitoes from the



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island of New Guinea to northern Australia in1998 (100).

PREVENTION ANDCONTROL OF JEV

The prevention and control of JEV trans-

mission can be achieved by three possiblestrategies, each targeting a specific part of

the transmission cycle: (a) vaccination of thehuman population, (b) control of amplifying

hosts by either swine vaccination or changesin animal husbandry, or (c) vector control.

Human vaccination is considered the mostreliable method of preventing JE in humans.

Vaccination

Until recently, the only vaccine available inter-nationally and recommended for travelers was

the mouse brain-derived, formalin-inactivatedvaccine developed using the prototype

Nakayama strain, which was manufacturedand exported by the Biken Institute in Japan

(113). Similar vaccines were manufactured inChina, Japan, Korea, Taiwan, India, Thailand,

and Vietnam (27). Use of this vaccine hasalmost eliminated the incidence of disease

in Japan, Korea, and Taiwan (46, 115, 150),

although other activities such as vector controland alternative agricultural practices have all

contributed to the reduction in disease (46).Inactivated cell culture vaccines prepared in

primary hamster kidney (PHK) or Africangreen monkey kidney (Vero) cells, and a live

attenuated SA14-14-2 vaccine have been usedin China (64). The SA14-14-2 vaccine has

also been used successfully in Nepal (130), andmost recently in India (3). The latter recorded

some adverse events, although the WHOGlobal Advisory Committee on Vaccine Safety

(WHOGACVS) concluded that no serious ad-

verse 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 significant risk in using the inactivatedmouse brain-derived Biken vaccine, particu-

larly with regardto neurological andallergicactions (125). Indeed, the Japanese governm

stopped recommending its use following a sgle case of acute disseminated encephalomy

tis after vaccination. However, as the link tween the vaccine andthis severe reaction co

not be definitively proven, the WHOGAC

concluded that there was no reason to chancurrent immunization recommendations (14

Despite this, manufacture of the Biken vcine was discontinued in 2005, necessitat

the development of suitable replacement vcines. Currently, a number of vaccines are u

der development or in clinical trial for intnational use (3). These include the inactiva

Vero-cell-derived SA14-14-2 vaccines (66, 1and a live attenuated chimeric vaccine based

the ChimeriVax infectious clone of 17D yellfever vaccine containing theprMandEgene

SA14-14-2 virus (78). These vaccines, togeth

with the potential licensing of the SA14-1attenuated vaccine in the future, suggest th

replacements for the discontinued Biken vcine will soon be available.

Control Measures TargetingVertebrate Hosts

Some protection against swine abortion is

forded by vaccination of sows (56). Howevswine vaccination is not effective or practi

for preventing transmission to humans. Becamost pigs are slaughtered at 68 months of a

annual vaccination of newborn piglets is quired and maternal antibodies render the li

attenuated vaccine ineffective against pigs lthan 6 months of age (46). The reduction

JE incidence in Japan, Taiwan, and Korea been partially linked to the relocation of d

mestic pigs to specialized farms sited away frhuman habitation (120, 136, 150). Finally

Japan, vaccination of horses has been carr

out during the JEV transmission season eayear since 1948 (82), resulting in a decrease

incidence of equine encephalitis (29). Indevaccination of race horses is mandatory in s

eral countries, including Singapore, Malayand Hong Kong.



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Mosquito Control

Although ultralow-volume insecticide applica-

tion 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 habi-

tats for Cx. vishnuisubgroup mosquitoes, cou-pled with the isolation of rural villages, makeit virtually impossible to employ large-scale

chemical treatment to control JEV transmis-

sion (62). However, the widespread applica-tion of pesticides to control agricultural insects

has had the added benefit of also reducingmosquito populations (61, 76, 150). Indoor

residual spraying using DDT and other chem-icals to control malaria is largely ineffective

in reducing JEV transmission, owing to the

largely exophilic resting behavior of the vectormosquitoes, although JE incidence was reducedin China, where pyrethroid-impregnated bed

nets were deployed (65). In most JEV endemicrural settings, where vaccination rates are of-

ten low, an integrated vector management ap-

proach incorporating alternating wet and dryirrigation and larvivorous fish can reduce vec-

tor populations and potentially JEV transmis-sion (54, 62).

THE SPREAD OF JAPANESEENCEPHALITIS VIRUS

In common with other members of the JEV

serological complex, JEV has shown a propen-sity 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 re-

cently 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

Culex sitienssubgroup: a group morphologicallysimilar species withithe subgenus Culex(Culex), from which

Cx. annulirostrisis thprimary AustralasianJEV vector

spread the virus regionally (70). Viremic mi-gratory birds (84) and even bats, especially

fruit bats (Megachiroptera) (2, 122), may beinvolved in distant transport. Wind-blown in-

fected mosquitoes have been suggested for the

dispersalofJEVinChina(72)andintoAustralia(100). The incidental transport of infected

mosquitoeson aircraft hasbeenimplicated(38),and it has been suggested that Japanese troop

movements in World War II may have intro-duced JEV into areas of Southeast Asia, possibly

via transport of infected mosquitoes in aircraftor equipment, or via infected pigs (70). Rice

irrigation and fertilizers that have resulted inincreased vector populations, and increased pig

production, have all been associated with thespread and establishment of JEV in new areas

(54, 70, 132).

The Australian Experience

While JEV has recently appeared in Australia, it

is noteworthy that after more than 10 years, thevirus has apparently not become established on

the mainland, let alone spread beyond the re-gion. This is despite predictions that when JEV

first appeared in a widespread outbreak on theTorres Strait islands in 1995 (37), it was feared

thatitwouldspreadtothemainlandsCapeYork

Peninsula, where populations of feral pigs, wad-ing birds, and mosquitoes were prolific (67). In

light of the explosive spread of WNV in theAmericas, the apparent inability of JEV to es-

tablish warrants a detailed discussion.When compared to the Torres Strait islands,

where intense activity has resulted in repeatedmosquito isolates and widespread rapid sero-

conversion of pigs, recorded JEV transmissionhas been of a low level on Cape York Peninsula.

First, fewer domestic pigs are housed in CapeYork Peninsula communities and seroconver-

sion of these pigs to JEV during two incur-

sions of JEV into Cape York Peninsula in 1998and 2004 has been asynchronous, thus limit-

ing the pool of available epizootic hosts (36).Second, collections of 48,495 Culex sitienssub-

group mosquitoes on Cape York Peninsula in1998 and 2004 yielded only one JEV isolate



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(in 2004) (138, 139), whereas comparable col-lections 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 ev-

idence of human JEV infections on Cape YorkPeninsula from serosurveys of 1092 individuals

in seven communities following the 1998 out-break (36). Furthermore, no JEV activity has

been detected in mainland sentinel pigs in yearsfollowing the Cape York Peninsula incursions

(139). Although it is possible that some JEVtransmission is cryptically maintained in foci on

Cape York Peninsula, JEV certainly has not be-come a significant public health issue on the

Australian mainland.Several mechanisms have been proposed to

account for the failure for JEV to become estab-

lished on the Australian mainland. Cape YorkPeninsula has several endemic flaviviruses, such

as KUNV, MVEV, and Kokobera virus (50,138), that might cross-protect pigs from infec-

tion with JEV (36). However, JEV cocirculateswith related flaviviruses in Papua New Guinea

(52) and India (101). Different lineages ofCx. annulirostris occur on Cape York Penin-

sula and southern Papua New Guinea and maydiffer in their vector competence for JEV. In-

deed, there is preliminary evidence to suggestthat the most widely distributed mainland Aus-

tralian lineage ofCx. annulirostrisis a relatively

inefficient laboratory vector of genotype I JEVthat has been circulating in northern Australia

since 2000 (40).The presence of alternative hosts may serve

to minimize blood feeding by Cx. sitiens sub-group mosquitoes on feral pigs. Analysis of host

feeding patterns revealed that only 5% and 1%ofbloodfed Cx.sitienssubgroup mosquitoes col-

lected from rural locations on western CapeYork Peninsula had fed on birds and pigs, re-

spectively (137). Most (75%) of these bloodmeals were of marsupial origin and were ret-

rospectively identified to be from the agile

wallaby (Macropus agilis) (142), which is abun-dant on Cape York Peninsula but absent from

most Torres Strait islands. When experimen-tally inoculated with JEV, both Tammar walla-

bies (Macropus eugenii) and agile wallabies faito develop a viremia (69). Indeed, if agile w

labies are an unsuitable JEV host, then prerential blood feeding byCulex on this spec

could effectively dampen transmission and pvent virus maintenance (137). The only ar

on Cape York Peninsula where JEV has be

detected in pigs or mosquitoes had local cocentrations of domestic or feral pigs, accom

nied by a high incidence of blood feeding bysitienssubgroup mosquitoes on pigs (137, 13

POTENTIAL EMERGENCEAND PUBLIC HEALTH RISKTO REGIONS OUTSIDE ITSNATURAL RANGE

Considering its propensityto spread, JEV co

become established in new ecosystems outsof its current range. However, unlike the rec

expansion into India and Australasia, whoverlapping natural cycles are thought to h

introduced the virus, JEV would have to tverse great distances over the Pacific Oce

the Indian Ocean, and the deserts and moutains to the northwest of Pakistan to inf

the Americas, Europe, or Africa. Introductby migratory birds is plausible, although t

migration routes of ardeid birds are genera

north-south rather than east-west, and biwould no longer be viremic after the lo

journey from Asia. Instead, human-transpormosquitoes or viremic vertebrates would

more likely mechanisms, as has been propofor the potential introduction of WNV in

Hawaii from the United States (55). Howevowing to animal quarantine procedures and

short duration of viremia in birds and pigs, most likely mechanism of introduction wo

be via an infected mosquito transported by acraft from a JEV endemic area. Indeed, h

populations of adultCx. tritaeniorhynchusoc

near Narita International Airport, Japan, athis species has been collected in aircraft ori

nating from other locations in Asia (38).Should JEV be introduced into a new

gion, a range of factors will influence its tablishment, as illustrated using a hypotheti



11/21

North American scenario. The areas at po-tentially greatest risk are those with intensive

pig rearing, such as the Midwestern UnitedStates, where swine populations exceed 30 mil-

lion head (83). However, many of these are

reared within purpose-built buildings and maynot be exposed to significant mosquito feeding,

andthe Australian experience suggests that JEVmay be unable to establish itself in areas if vec-

tors cannot or do not access significant swinepopulations.

For it to establish, JEV may have to ex-ploit native or introduced vertebrate species in

muchthesamewayasWNV,forwhichendemicbirds (57), reptiles (49), and mammals (88) have

been implicated in transmission cycles. Nu-merous species of ardeid wading birds occur

in North America, including widespread resi-

dent populations ofN. nycticorax and the cattleegret(Bubulcus ibis),twospeciesinvolvedinJEV

transmission in Asia (98). Other bird speciescommon to both Asia and North America,

including English sparrows, house finches, pi-geons, ducks, and chickens, produce viremia af-

ter experimental infection (15, 19, 35). How-ever, these bird species do not contribute to

epidemic JEV transmission to the same extentas ardeid birds and pigs, possibly because they

only produce a low-level viremia, andCx. tritae-niorhynchusrarely feeds on them. Nonetheless,

there are guilds of ornithophilic Culex species

(77) that may facilitate enzootic transmissionthrough 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 en-

demic flaviviruses, such as SLEV and WNV,may provide some level of immunity against

JEV, thus reducing the pool of available hosts tofacilitate enzootic transmission. However, the

cocirculation of JEV and MVEV in Papua NewGuinea, and of JEV and WNV in Pakistan,

suggest that sufficient populations of suscepti-

ble hosts exist to allow concurrent circulationof these closely related flaviviruses in the same

ecosystem (52, 101).

A number of secondary or moderately sus-ceptible JEV vectors already occur in North

America, including Cx. pipiens, Cx. quinquefas-ciatus,Ae. albopictus,Ae. japonicus, andAe. vexans.

However, endemic Culex spp. are more likelyto be involved in local transmission, especially

vectors of endemic JEV serological group fla-

viviruses, such as Cx. tarsalis, Cx.pipiens, Cx.sali-

narius, and Cx. nigripalpis. Vector competence

experiments with North American mosquitoesconducted in the 1940s not only confirmed thatCx. tarsalisand Cx. pipienscould serve as labora-tory vectors of JEV but also incriminated non-

Culex species, including Ae. dorsalisand Culisetainornata (94).

The introduction and establishment of JEVin a virgin ecosystem, such as the United States,

could have dramatic consequences for humanand animal health. JEV has a higher rate of se-

vere neurological disease compared with other

endemicencephaliticflaviviruses,suchasSLEVand WNV (134, 135). Additionally, SLEV and

WNV more often cause severe disease in theelderly, whereas both children under 5 years

of age and the elderly typically develop se-vere clinical manifestations following JEV in-

fection. Furthermore, when JEV emerges inan immunologically nave population, clinical

disease occurs in all age groups (13, 41). Fi-nally, in terms of animal disease, significant

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 neces-sary to limit the potential impact of JEV should

it emerge in a region outside of its current geo-graphical distribution. This plan shouldinclude

an active surveillance system, comprising hu-man and animal clinical case diagnosis, cou-

pled with JEV-specific diagnostic assays forrapid detection of an incursion. Should the

virus become established, control programs willhave to be implemented, potentially at signifi-

cant economic cost to all levels of government.

Widespread immunization of residents at risk



12/21

maybe needed, with introduction of the vaccineinto the early childhood vaccination schedule.

Tourism could be affected, especially if vacci-nation is recommended for travelers visiting

endemic areas, as is the case with visitors to

Southeast Asia (113). The economic impact onagriculture would also be considerable, as there

would be concerns regarding the export of live-

stock and associated products, resulting in a quirement for widespread testing to verify fr

dom from infection. Importantly, the potenrole that endemic mosquitoes and vertebr

species could play in transmission cycles ne

to be assessed using laboratory-based infectand transmission experiments before an o

break 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. JEVismaintainedinanenzooticcyclebetweenardeidwadingbirdsand 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 birdsand/or bats and wind-assisted dispersal of mosquitoes may reintroduce the virus.

6. Control measures include human vaccination and, to a limited extent, alternative pighusbandry and vector control.

7. While JEV has expanded its range into northern Australia, it does not appear to havebecome established in natural transmission cycles. Possible reasons for this include (a)the

presence of related flavivirusesthat may providecross-protection against JEV infection insusceptible hosts; (b) different lineages ofCx. annulirostris, which may vary in their vector

competence to the different genotypes of JEV; and (c) a propensity for Cx. annulirostristo 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 difficult, and modern pig husbandry may impedevirus amplification.

FUTURE ISSUES

1. Modeling should be used to investigate why JEV has failed to establish in mainlandAustralia, 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 conductingvector competence experiments with native mosquito species, especially those belonging

tothegenus Culex. In addition, conducting laboratory-based infection studiesof common



13/21

vertebrate fauna with JEV may determine their potential role in JEV transmission cy-

cles. This will provide information to facilitate a targeted response should the virus beintroduced.

3. The genetic basis for the variation in vector competence between populations of

Cx. tritaeniorhynchusand other vector species should be investigated.

4. Culex ecology, especially blood-feeding behavior, near modern intensive pig-rearing fa-

cilities or ardeid roosts should be investigated.

5. It should be assessed whether infection of vertebrates with endemic flaviviruses, including

MVEV, WNV and SLEV, provides cross-protection or immune enhancement followinginfection with JEV.

6. More specific serological assaysarerequired to differentiate JEV from related flaviviruses.

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 Healthand Tony Sweeney for preparation of the figures, and Richard Russell, Roy Hall, Cassie Jansen,

and Jay Nicholson for reviewing a draft of the manuscript. We also thank Marc Klowden and DanKline during the genesis of ideas presented in this review.

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