Emerging infectious diseases in wildlife

IntroductionDuring the current period of increasing globalisation, theemergence of new diseases of wildlife or the re-emergence ofold diseases should not be surprising (34). The world is

undergoing rapid ecological change, populated by pathogenicorganisms, their vectors and hosts which are capable of equallyrapid change. Some of these pathogens may cause significantdisease in wild species, but in other cases, the wild animals mayserve as reservoirs for pathogens which do not induce overtillness in their wild hosts.

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Emerging infectious diseases in wildlife

SummaryThe processes which give rise to emerging infectious diseases of wildlife can becategorised as follows: ecosystem alterations of anthropogenic or natural origin;movement of pathogens or vectors, via human or natural agency; and changes inmicrobes or in the recognition of emerging pathogens due to advances in thetechniques of epidemiology. These are simplistic divisions because factorsinfluencing the emergence of diseases of wild animals generally fall into morethan one category. Mycoplasmosis among passerines is related to habitatchanges and artificial feeding resulting in increased bird densities andsubsequent disease transmission. The origin of this strain of Mycoplasmagallisepticum is not known. Hantavirus infections in rodents have emerged dueto human-induced landscape alterations and/or climatic changes influencingpopulation dynamics of hantavirus reservoir hosts, with disease consequencesfor humans. Movement of pathogens or vectors is a very important process bywhich diseases of wildlife expand geographic range. Although the origin ofcaliciviruses of rabbits and hares is somewhat obscure, their movement byhumans, either deliberately or accidentally, has greatly expanded the distributionof these viruses. Rabies is an ancient disease, but geographic expansion hasoccurred by both natural and anthropogenic movements of wild animals. Humanmovement of amphibians may explain the distribution of the highly pathogenicchytrid fungus around the world. Newly recognised paramyxoviruses may reflectboth changes in these pathogens and the development of techniques ofidentification and classification. Many more such examples of emerging diseaseswill arise in the future, given the extensive alterations in landscapes world-wideand movements of animals, vectors and pathogens. Those who study anddiagnose diseases of wildlife must be alert for emerging diseases so that theimpact of such diseases on wild animals, domestic animals and humans can beminimised.

KeywordsCaliciviruses – Chytridiomycosis – Emerging diseases – Hantaviruses – Mycoplasmosis –Paramyxoviruses – Rabies – Wildlife.

E.S. Williams (1), T. Yuill (2), M. Artois (3), J. Fischer (4) & S.A. Haigh (5)

(1) Department of Veterinary Sciences, University of Wyoming, 1174 Snowy Range Road, Laramie, Wyoming82070, United States of America(2) Institute for Environmental Studies, University of Wisconsin, Madison, Wisconsin 53706, United States ofAmerica(3) Département de santé publique vétérinaire, Unité de pathologie infectieuse, École Nationale Vétérinaire deLyon, B.P. 83, 69280 Marcy l’Étoile, France(4) Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia,Athens, Georgia 30602, United States of America(5) Canley Heights Veterinary Surgery, Cnr Harden and Avoca Street, Canley Heights, New South Wales 2166,Australia

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Emerging infectious diseases have been defined by Morse (90)as follows:

a) those diseases which have appeared in a population for thefirst time, or

b) those diseases which have existed but are rapidly increasingin prevalence or geographic range.

Although the term ‘emerging disease’ has been embraced by thebiomedical community and the media as a useful way tocategorise some diseases of humans and other animals, the termis perhaps overused. ‘Emerging disease’ has become nearlysynonymous with epidemic or epizootic in the literature and ingrant applications. However, some categories of diseasesaffecting or involving wild animals clearly meet the definition of‘emerging’. This classification can assist in understanding thesediseases, in developing methods for control and management,and in preventing the emergence of new diseases of wildlife.

Factors surrounding the emergence of infectious diseases ofwildlife fit into several categories. These have been bestdescribed for human diseases (90), and have also been appliedto other animals, particularly domestic species (16). Broadly,these categories include the following:

a) ecosystem alterations of anthropogenic or natural origin

b) movements of pathogens or vectors, via human or naturalagency

c) changes in microbes or in the ability to recognise emergingpathogens due to advances in the techniques of epidemiology.

Clearly, factors influencing emergence of many of the diseasesof wild animals fall into more than one category.

Alteration of ecosystems can create conditions which facilitatethe appearance and spread of new diseases. The duck plagueoutbreak at Lake Andes, South Dakota, United States ofAmerica (USA), is an example of the way in whichenvironmental management created conditions for theoutbreak of a new disease. Waterfowl managers kept lake wateropen during the winter, which attracted large numbers of ducksand geese. Duck plague virus, a herpesvirus which had beenrecognised in the domestic duck industry in Long Island, NewYork, USA, in 1967, unexpectedly appeared at Lake Andes in1973 and rapidly killed over 43,000 ducks and geese (140).Similarly, the creation of artificial water holes in Etosha NationalPark, Namibia, created a situation resulting in repeated cases ofanthrax in large wild mammals (72).

Situations which favour disease appearance can also occurinadvertently. Hardwood trees cut in south-western Wisconsin,USA, form basal tree holes which collect water and increase thenumbers of breeding sites for Aedes triseriatus, the naturalmosquito vector of La Crosse virus. The reservoir of the virus issmall forest mammals. The virus is also transmitted to humans,causing encephalitis, principally in pre-school age children

(126). Reforestation of the north-eastern USA favouredtransmission of Lyme borreliosis due to increased populationsof white-tailed deer (Odocoileus virginianus) and deer mice(Peromyscus leucopus), and abundance of the tick vector, Ixodesscapularis (17). In these cases, clinical disease is apparently nota feature of infection of the wild animal host, but these animalsserve as reservoirs of the pathogens for domestic animals andhumans.

Natural climatic changes can increase host abundance andtransmission of pathogens, as in the case of Sin Nombrehantavirus in the south-western USA. Increased rainfallresulted in more grass setting seed and expansion of rodent(Peromyscus spp.) populations which are natural reservoirs ofthe virus, and thereby greater human contact with these miceand their excretions (42). This resulted in virus transmission tohumans and the appearance of hantavirus pulmonarysyndrome (HPS). Although the virus was undoubtedlyendemic in rodent populations for centuries, causing sporadiccases of human HPS, the aetiology was undiscovered until1993 (112).

Movement of pathogens often occurs within animal hosts andthis can have significant impacts on naïve populations. Theinteraction of wild and domestic species can result in seriousoutbreaks of disease in wildlife. The epizootic of rinderpest inAfrica in the 1890s is one of the most dramatic examples of adisease transmitted from domestic livestock to a virginpopulation of wild ungulates, with resultant high mortality(113). More recently, the appearance and rapid spread ofmycoplasmal conjunctivitis in wild songbirds raised questionsregarding the possible transmission of Mycoplasma gallisepticumfrom backyard poultry to wild birds, although significantantigenic differences between M. gallisepticum in wild birds andisolates from commercial domestic poultry operations tend torule out that source of the epornitic (44).

Movement of pathogens has also accounted for the appearanceof wildlife diseases in new areas. Translocation of infected wildand domestic animals has been an important factor in theappearance of epizootics of rabies in new locations. Rabiesapparently was introduced into the New World by infecteddogs in the early 18th Century, with subsequent spillover intoa variety of wild terrestrial mammals. More recently, rabiesbecame established in racoons (Procyon lotor) in the mid-Atlantic states of the USA in the late 1970s, due to illegaltranslocation of racoons into the region from the south-eastUSA, where rabies was endemic in this species. Racoon rabiescontinues to spread into the north-eastern (110) and mid-western USA. The domestic dog strain of rabies virus may havebeen introduced from Europe to southern Africa, and henceinto wild canids.

However, the emergence of rabies across continental Europemay have resulted in geographic expansion because of changesin host populations, including numbers and species, but was

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probably not due to translocations. The surprising appearanceof disease due to West Nile virus in humans, horses, and wildbirds in New York, and the subsequent spread along theAtlantic coast, is a very recent example of introduction andestablishment of a pathogen which apparently originated in theMiddle East. The mechanism of introduction into the USA isunknown (20).

Although the origin of chronic wasting disease (CWD), aspongiform encephalopathy of deer and elk, is not known,movement of Rocky Mountain elk (Cervus elaphus nelsoni) inthe commercial game farm industry, has resulted in a greatlyexpanded geographic distribution of CWD. The disease hasnow been identified in privately-owned elk in six states of theUSA, in one province of Canada, and very recently, in theRepublic of Korea. The occurrence of CWD in the game farmindustry in Canada appears to have resulted in transmission ofthe disease to free-ranging mule deer (Odocoileus hemionus) inSaskatchewan, although this is still under study. A morecomprehensive discussion of CWD is provided in this issue ofthe Review (139).

Movement of vectors can also contribute to the appearance ofdiseases involving wildlife reservoirs. Ixodes scapularis, thevector of Lyme borreliosis in North America, was found in theupper Midwest for the first time in 1968. The tick hassubsequently spread in this region, probably due to transportby wild birds (17).

Infectious diseases have been introduced deliberately into pestwildlife populations as a means of population control. Theclassical examples of the introduction of highly fatal viruses intopopulations of an extremely susceptible host species are thoseof myxomatosis and rabbit calicivirus into populations ofEuropean rabbits (Oryctolagus cuniculus) in Australia (43, 68).

The contribution of exposure of wildlife to anthropogeniceffluents and toxicants to the appearance of new infectious andparasitic diseases is not well understood. In 1993, an estimated100,000 different chemicals were used annually world-wide(94). The effects that these chemicals may have, alone or incombination, on immune modulation and susceptibility toinfectious and parasitic diseases awaits further study. Inaddition, these chemicals may cause alterations in habitats,influencing animal and microbial numbers and distribution,resulting in increasing impact of pathogens. Some examplesinclude possible association of agricultural run-off with bloomsof the dinoflagellate Phiesteria piscicida and disease in fish alongthe southern Atlantic seaboard of the USA (18), and the seriousimpact of Eustrongylides ignotus, a nematode parasite, on wadingbirds in Florida, associated with alterations to the food chaindue to nutrient effluents in canals and ponds (116).

Mutation and recombination of pathogens can give rise to newpathogens, or modification of existing ones. New pathogenscan arise through recombination. For example, the threeribonucleic acid (RNA) segments of bunyaviruses such as La

Crosse and Jamestown Canyon can give rise to six distinctreassortants in dually infected mosquitoes (23). The RNA issubject to frequent mutations and there are no editingmechanisms to repair the changes (63). Changes which appearto be mutational may be phase variation in which genes suchas those that code for antigens, which have been part of thegenetic repertory, but silenced, are suddenly reactivated (63).Activating and resilencing genes which code for antigens canprovide pathogenic parasites and bacteria with a mechanism toescape the immunological defences of the host. Bacteria canexchange genetic material through plasmid interchange, a wellrecognised mechanism which permits the spread of antibioticresistance genes among widely differing species of bacteria.

As the powerful tools of molecular characterisation ofpathogens are improved, a better understanding of theepidemiology of some of these agents is obtained. Applicationof these techniques to pathogens such as Ehrlichia has revealedthe involvement of wild animals and humans. Thus, thesediseases may not be new, but their epidemiological stories arenow better appreciated (37).

The remainder of this review paper discusses some importantexamples of emerging diseases of wildlife. The discussion is byno means comprehensive because many other wildlife diseasesfit within the definitions of ‘emerging disease’. The intent is todescribe in greater detail a few wildlife diseases from around theworld which represent good examples of the factors associatedwith disease ‘emergence’ in wild species.

Ecosystem alterations ofanthropogenic or natural originMycoplasmal conjunctivitis of wild finchesEpornitic conjunctivitis in house finches (Carpodacusmexicanus) was first reported in suburban Washington DC,USA, during the winter of 1993-1994 when large numbers offinches with swollen, crusty eyelids and nasal exudate wereobserved at backyard feeding stations (Fig. 1). The vision of thebirds often was impaired and they were debilitated, reluctant toleave feeding platforms, and easily captured by hand.Mycoplasma gallisepticum was subsequently isolated fromconjunctival swabs of affected finches (69, 78). Althoughantibodies against M. gallisepticum previously had been detectedin wild birds associated with poultry facilities in the USA (120),M. gallisepticum had never been associated with clinical diseasein wild passerines. Mycoplasmal conjunctivitis was observed inhouse finches in nine mid-Atlantic states by October 1994 andthroughout the entire eastern range of the species by 1996 (44).To date, house finches with conjunctivitis have been reportedalong the Atlantic coast from Quebec, Canada, to Florida andwestward from North Dakota to Texas.

House finches are sparrow-sized birds native to the westernUSA. Capture and transport of finches from the western states

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for commercial sale in the eastern states occurred in the early20th Century and the birds were introduced to Long Island,New York, in about 1940 (41). House finches multiplied andspread and now are common backyard birds throughouteastern and mid-western North America. Although the easternhouse finch population now extends to the range of the westernpopulation, mycoplasmal conjunctivitis has not been reportedin western house finches.

Since 1995, conjunctivitis due to M. gallisepticum infection hasbeen confirmed in other wild birds, including the Americangoldfinch (Carduelis tristis) (Fig. 2) (44, 70), purple finch(Carpodacus purpureus) (48), pine grosbeak (Pinicolaenucleator), and evening grosbeak (Coccothraustes vespertinus)(87). Mycoplasmal conjunctivitis in goldfinches and a purplefinch has involved only a few scattered individuals suggestingspillover from house finches. However, in early 1999, 10%-20% of pine grosbeaks and evening grosbeaks at feedingstations in north-eastern Quebec were affected by conjunctivitis(87). Isolates of M. gallisepticum from house finches and otheraffected species have been genetically indistinguishable,suggesting that M. gallisepticum was transmitted from a singlesource throughout wild bird populations. This strain ofM. gallisepticum differs from strains often associated withmycoplasmal disease in domestic poultry as well as those usedin poultry vaccines. The origin of the finch M. gallisepticumstrain remains unknown (70).

The rapid spread of mycoplasmal conjunctivitis throughout therange of the eastern house finch probably reflects both birdbehaviour and human activity (44). House finches are welladapted to human land use practices and prefer to nest andfeed around buildings and farms as well as in suburban areas.During the winter, house finches often flock to bird feedingstations where transmission of infectious disease agents is

enhanced via direct contact, and an increased prevalence ofaffected finches has been reported during this season (49).Although precise modes of M. gallisepticum transmission amongwild finches are unknown, contamination of feeder surfaceswith M. gallisepticum has been documented and may serve as asource of infection for finches (47). Additionally, eastern housefinches, unlike their western counterparts, may migrate severalhundreds of miles and could therefore disseminate a diseaseagent over a large geographic area (6).

Mycoplasma gallisepticum has long been recognised as asignificant pathogen of domestic poultry and farmed gamebirds. The organism is the cause of chronic respiratory diseasein chickens and infectious sinusitis in turkeys (71). On rareoccasions, M. gallisepticum has caused infectious sinusitis inwild turkeys closely associated with domestic poultryoperations (36). Keratoconjunctivitis due to infection withM. gallisepticum has been reported in chickens (99) as well as infarmed game birds such as pheasant (Phasianus colchicus) andchukar partridge (Alectoris chukar) (30). The M. gallisepticumstrain of wild finches infected and elicited an antibody responsein domestic chickens and turkeys exposed to the organismexperimentally, but clinical disease was mild, if present at all(101). In another experimental trial, M. gallisepticum wastransmitted from naturally-infected house finches to chickens,but transmission required an extensive contact period (tenweeks) and clinical disease was not apparent during the study(121).

Conjunctivitis in wild birds may be detected via observation ofbirds at backyard feeding stations and other sites. Indeed,observation of birds at feeders was used successfully todocument the spread of mycoplasmal conjunctivitis via aunique public survey known as the House Finch DiseaseSurvey of the Cornell Laboratory of Ornithology (38). The


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Fig. 1Extensive conjunctival inflammation, periorbital alopecia, andnasal exudation in a house finch with Mycoplasmagallisepticum infection

Fig. 2Conjunctivitis in an American goldfinch with Mycoplasmagallisepticum infection

survey facilitated an investigation of disease trends across largegeographic areas which would have been impractical bytraditional means.

Diagnosis of mycoplasmal conjunctivitis can be confirmed onlyby culture; however, clinical signs, gross and microscopiclesions, serological testing, and molecular techniques canprovide a strong preliminary diagnosis. Gross lesions ofM. gallisepticum in house finches consist of unilateral or bilateralconjunctival swelling with serous to mucoid ocular and nasaldischarge, crusts of dried exudate at the eyes and nares, andperiorbital alopecia due to self-trauma (79). Chronically andseverely affected birds may be thin. Microscopic lesions consistof chronic inflammation of the ocular and upper respiratorytissues (44, 79). Moderate to severe lymphoplasmacyticinflammation, lymphoid hyperplasia, and epithelial hyperplasiaare present in the conjunctiva, and mild to moderate keratitis isobserved in some cases. Unilateral rhinitis is often present andis characterised by mucosal necrosis, lymphoplasmacyticinflammation, and hyperkeratosis of nasal turbinates. In fewercases, chronic, lymphoplasmacytic tracheitis is observed.Transmission electron microscopy reveals adherentmycoplasmal organisms on epithelial surfaces.

The serum plate agglutination (SPA) test is the serological assayof choice for screening birds for M. gallisepticum antibodiesbecause it is simple, inexpensive, and can be used for manyavian species (58). The SPA test detects the earliest antibodyresponse produced and remains sensitive for a long period oftime; however, it has low specificity resulting in possible falsepositives. Serological tests with higher specificity, such as thehaemagglutination inhibition test and enzyme-linkedimmunosorbent assay (ELISA), should be used to confirm SPA-positive samples (58). However, problems arise in applyingthese tests to wild birds, due to difficulties in test interpretationand disparities in reagents.

Polymerase chain reaction (PCR) techniques are sensitive andtimely alternatives to culture of M. gallisepticum. Specificoligonucleotide primers are used to amplify small amounts ofnucleic acid to detectable levels (60). Random amplification ofpolymorphic DNA (RAPD) or arbitrary primed PCR generateDNA fingerprints which are used for molecular typing of strains(70, 79). These techniques are valuable for molecularepidemiological studies.

For culture of M. gallisepticum from affected birds, swabs of thetrachea, conjunctiva, choanal cleft, or infraorbital sinus areplaced into liquid growth media and incubated. Mycoplasmagallisepticum is a fastidious organism which requires a complexselective medium enriched with animal serum, dextrose, and ayeast source. Frey’s medium with swine serum (FMS) isfrequently used (58). Other media used with success includeSP4 (138), PPLO (58), and Edward-type (15). Broth and agarmedia are prepared with these formulations; penicillin andthallium acetate may be added to inhibit growth of bacterial

and fungal contaminates. The broth is incubated until growthis indicated, then plated on agar for identification procedures.

As with many diseases in free-ranging wildlife, mycoplasmalconjunctivitis of wild birds is not easily treated or managed.Individual birds may be captured and treated withantimicrobial agents (136). However, this practice is of nobenefit to wildlife populations, and should therefore bediscouraged; chronically infected birds without clinical diseasemay be released and serve as reservoirs of M. gallisepticum in thewild, and M. gallisepticum has been transmitted from affectedhouse finches to other species in rehabilitation facilities (69).Basic measures to lower potential disease risks at bird feedersmay reduce the transmission of mycoplasmosis in passerines(77). Feeding stations should be cleaned and disinfectedregularly as well as spaced to reduce crowding. Only clean andunspoiled feed should be used and spilled waste beneathfeeders should be cleaned up. If a local outbreak ofmycoplasmosis occurs, a temporary cessation of feeding mayhelp to disperse healthy birds before they become exposed. Inaddition, physical contact between backyard domestic poultryand wild birds should be prevented.

The ultimate impact of mycoplasmal conjunctivitis on wild birdpopulations is uncertain. Since the beginning of the epornitic ofM. gallisepticum infection, house finch populations in severaleastern states have declined dramatically in areas where birdsoccurred at high densities prior to the outbreak; however,populations with lower densities have remained stable,suggesting density-dependent transmission of M. gallisepticum(53). Five years after the epornitic began, M. gallisepticumremains endemic in eastern house finches, but appears to havedeclined in prevalence (49). Although several cases of clinicalconjunctivitis have been observed in goldfinches, purplefinches and house sparrows (Passer domesticus) in the easternUSA, population declines have not been apparent in thesespecies (50). Other healthy wild birds have been positive forM. gallisepticum antibodies, and tufted titmice (Baeolophusbicolor) were positive by PCR, suggesting that this species maybe a subclinical carrier of M. gallisepticum or a closely relatedmycoplasma (80).

HantavirusesHantaviruses, members of the Bunyaviridae family, are found inrodent reservoirs, and one insectivore, world-wide (Tables I, IIand III). Twenty-six distinct hantaviruses have been identified(88). These viruses establish asymptomatic, persistentinfections in their rodent or insectivore hosts, but are theaetiological agents of haemorrhagic fever with renal syndromeof variable severity (83) in humans in Asia and Europe, and ofHPS in the Americas. Hantaan virus, the prototype of thegroup, is the aetiological agent of Korean haemorrhagic fever(64) and has caused thousands of cases annually in the People’sRepublic of China. The closely related Seoul virus causes milderhaemorrhagic disease and is distributed world-wide in theNorway rat (Rattus norvegicus) through internationalshipping (65).


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Hantavirus pulmonary syndrome was first recognised in thesouth-western USA in 1993, and deer mice (Peromyscusmaniculatus) were demonstrated to be the reservoir (24).Subsequently, other hantaviruses in a variety of rodents of theSigmodontinae family were shown to cause human HPS in theWestern Hemisphere. Precipitation, habitat structure, and foodavailability are implicated as critical environmental factorswhich affect rodent population dynamics as well as viraltransmission and persistence (1). Rodent hosts shed variableamounts of these viruses in faeces, urine and saliva over longperiods of time. Infection in rodent hosts may persist despitethe presence of neutralising antibody. Bite wounds inflictedduring fighting appear to be a major mode of virus transmissionamong rodents (88). Evidence exists for the direct human-to-human transmission of one hantavirus, Andes virus, inArgentina (137). Hantavirus infections are diagnosed byserological methods (principally indirect fluorescent antibody,enzyme immunoassay for immunoglobulin G [IgG] or IgM,and a rapid strip immunoblot assay which can be used in thefield [52]), virus isolation, and demonstration of the presenceof virus by immunohistochemistry or of viral RNA by reverse

transcriptase PCR (RT-PCR) (59). Rodent control andavoidance of contact with these reservoir hosts is the onlymeans to avoid infection of humans.

Movement of pathogens orvectors via human or naturalagencyCalicivirus diseases of rabbits and haresRabbit haemorrhagic disease (RHD) has been variously termedrabbit calicivirus disease, haemorrhagic tracheitis of rabbits,haemorrhagic pneumonia of rabbits, necrotic hepatitis ofrabbits, rabbit plague, rabbit viral sudden death, and rabbit Xdisease (68), reflecting the pathological characteristics and signsof the disease. The disease first appeared in domestic rabbitriesin the People’s Republic of China in 1984, and later spread intoEurope, initially appearing in a severe epizootic in Italy in 1986,in the United Kingdom (UK) in 1992, and then into NorthAfrica, spilling over from domestic rabbits to wild Europeanrabbits with significant mortality in both (86). The diseaseappeared in domestic rabbits in Mexico in 1988, but wasrapidly eradicated (51).

After demonstrating that the RHD virus was specific for theEuropean rabbit host, the authorities responsible for rabbitcontrol in Australia conducted experiments in which rabbitswere exposed in large pens on Wardang Island (68). Althoughthese initial field trials on transmission of the virus amongpenned rabbits did not appear promising, the virus escapedfrom the island in 1995 and spread rapidly to disparate regionsof Australia, aided by deliberate introduction of the virus intowild rabbit populations by farmers and pastoralists.Unauthorised introduction of the disease into New Zealandoccurred in 1997. The virus spread directly among wild rabbitsor mechanically by arthropod vectors (67). Populationreductions of 65%-95% were recorded, and mortality has been


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Table IHantaviruses causing haemorrhagic fever with renal syndromein humans (88)

Virus (a) Known or suspected host Geographic distribution

Hantaan (a) Apodemus agrarius East Asia, Eastern Europe

Seoul Rattus norvegicus East Asia, seaports world-wide

Dobrava/Belgrade Apodemus agrarius Balkans, Eastern Europe

A. flavicollis (suspected) East Asia, Eastern Europe

Puumala (b) Clethrionomys glareolus Scandinavia, Europe, Western Russia

a) severe disease in humansb) mild disease in humans

Table IIIHantaviruses not known to cause disease in humans oranimals (88)

Virus Known or suspected host Geographic distribution

Prospect Hill Microtus pennsylvanicus North America

Bloodland Lake M. ochrogaster North America

Isla Vista M. californicus Western USA and Mexico

El Moro Canyon Reithrodontomys megalotis Western USA and Mexico

Rio Segundo R. mexicanus Costa Rica

Caño Delgadito Sigmodon alstoni Venezuela

Rio Mamore Oligoryzomys microtis Bolivia and Peru

Bermejo O. chacoensis North-western Argentina

Maciel Bolomys obscurus Central Argentina

Pergamino Akodon azarae Central ArgentinaTable IIHantaviruses causing hantavirus pulmonary syndrome inhumans (88)

Virus Known or suspected host Geographic distribution

Sin Nombre Peromyscus maniculatus West and Central USA(grassland form) and Canada

New York P. leucopus (eastern Eastern USAhaplotype)

Black Creek Canal Sigmodon hispidus Florida(eastern form)

Bayou Oryzomys palustris South-eastern USA

Juquitiba Unknown Brazil

Laguna Negra Calomys laucha Paraguay and Bolivia

Andes Oligoryzomys longicaudatus Argentina and Chile

Oran O. longicaudatus North-western Argentina

Lechiguanas O. flavescens Central Argentina

highest where adult rabbits predominate over less susceptibleneonates and juveniles in the population. Case fatalityapproaches 100% in susceptible adults. The few individualsthat do survive acquire lifelong immunity to subsequentinfection. Rabbit calicivirus disease has proved moderatelyeffective in controlling wild rabbits in Australia.

Sudden death of European rabbits in otherwise good bodilycondition suggests RHD. Definitive diagnosis is obtained bydemonstration of RHD virus antigen in spleen and liver cells byimmunohistochemistry or in tissue homogenates by ELISA,human red cell haemagglutination, or demonstration of viralRNA by PCR. Virus particles can be visualised by transmissionelectron microscopy of liver homogenate supernatants.Presence of RHD virus antibody can be demonstrated by ELISAor inhibition of human red cell agglutination (22, 68). As thevirus does not replicate in vitro in cell cultures, inoculation ofsusceptible rabbits is the best way to isolate infectious virus. Noeffective measures have been found to control the disease inwild rabbits. Translocation of individuals from areas whereepizootic RHD is occurring should be prevented if the objectiveis to avoid spread of the disease.

European brown hare syndrome (EBHS), which is caused by avirus related to RHD virus, has also been termed leporidcaliciviral hepatitis, viral hepatitis of hares, and acute hepatosis(68). The disease, characterised by acute liver necrosis, causedepizootics in European brown hares (Lepus europaeus). Thedisease was first described in Sweden in the early 1980s, butreports from the 1970s describe a disease with similar grosslesions in European hares which died in England and othercountries of Europe, well before the appearance of RHD. Brownand varying hares (Lepus timidus) are the only species shown tobe susceptible to this virus. Interestingly, European rabbitsinoculated with EBHS virus develop antibodies to the virus, butnot clinical disease. Similarly, European and varying haresinoculated with RHD virus do not develop disease either (62).Like RHD, EBHS produces mortality only in adult animals.Juvenile hares may have inapparent infections and developantibody. Comparison between RHD virus and EBHS virusisolates has shown only 53%-71% homology between thesetwo groups. Comparison among isolates within the RHD virusand EBHS virus groups has shown them to be 90% or morehomologous, indicating a distant relationship between, but notwithin the groups (66, 98). Diagnosis of EBHS is essentially thesame as for RHD. In common with RHD virus, EBHS virus doesnot replicate in cell cultures. Infected hares in nature mayexhibit abnormal behaviour and have been termed ‘crazyhares’; the hares may lose fear of humans and dogs, and run incircles (68). No effective measures are available to control EBHSin populations of wild hares. Translocation of individuals fromfoci of infection should be avoided.

Amphibian chytridiomycosis‘Chytrid’ is the common name used for a phylum of fungicharacterised by asexual reproductive spores (zoospores) which

swim by means of a posteriorly directed flagellum (75). Thephylum currently contains a single class, five orders, andapproximately 120 genera. Based on the ultrastructure of thezoospores and on sequences from the 18S ribosomal DNA(rDNA), Batrachochytrium is classified in the largest order, theChytridiales. Batrachochytrium dendrobatidis is a fungusbelonging to this phylum and appears in two forms, namely: aspherical sessile zoosporangium of 10 µm-40 µm in diameter,and a motile zoospore of approximately 2 µm in diameter. Themotile zoospore attaches to the substrate, develops rhizoids,and within four days becomes a zoosporangium. Zoospores arethen released as motile zoospores via discharge tubes.Zoospores can live for over 24 h and are infective to frogs andtadpoles (L. Berger, personal communication).Batrachochytrium is the only genus of chytrid known to containa species which is pathogenic to vertebrates. Zoosporangiagrow only in the superficial keratinised layers of the epithelium.In frogs, the fungus is most commonly found on the feet. Intadpoles, B. dendrobatidis is found initially in the keratinisedmouthparts, and once these are lost, the organism invades thenewly keratinised tissues of the tail and feet.

Studies on ultrastructural morphology suggest that isolatesfrom the USA, Central America and Australia are closely related(7, 76). Studies on sequences of the 18S rDNA of chytrids froma wild White’s tree frog (Litoria caerulea) from Australia and apoison dart frog (Dendrobates azureus) from America foundonly five different base pairs of 1,700 sequenced (T.Y. Jamesand colleagues, personal communication). This adds support tothe hypothesis that B. dendrobatidis is a newly emerged agent.

In Australia, B. dendrobatidis has been found in frogs since 1989and has been observed in the rainforests of southern, centraland northern Queensland and northern New South Wales. InQueensland, Victoria, and Western Australia, chytridiomycosismay have spread at approximately 100 km per year (3, 117,118). The organism has been reported from anurans inrainforests of Panama, in captive and wild frogs in the USA, andin anurans which died at high altitudes in Ecuador. Evidencehas been found to suggest that B. dendrobatidis caused massmortality and population declines in high altitude, streamdwelling rainforest anurans in protected areas of Queenslandand Panama (8).

The pattern of decline of many populations of frogs in Australiais consistent with an epidemic after the suspected introductionof B. dendrobatidis into numerous protected habitats after 1978.Batrachochytrium was thought to be associated with suddendeclines in stream dwelling frogs even though tadpolessurvived. Tadpoles can carry infections in their mouthpartsfrom soon after hatching until metamorphic climax when thebeaks are shed and fungal sporangia are rapidly redistributed tothe skin of the body. Batrachochytrium may be able to avoid itsown extinction, as it moves into and decimates a population, bysubclinical infection of tadpoles and/or survival as a saprobe(outside the amphibian host) (35). Healthy frogs also may be


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carriers of the fungus, and low levels of infection have beenfound in clinically normal frogs from the wet tropics inQueensland (R. Speare and M. Freeman, personalcommunication).

Two potential causes of emergence of B. dendrobatidis as asignificant pathogen have been suggested, namely: introductioninto naïve populations and climate change. Severalcharacteristic features of the population declines of highaltitude, stream dwelling rainforest amphibians from protectedareas in Australia (85, 108) and Central America (73)implicated a waterborne infectious disease: only streamdwelling frogs disappeared, no environmental changes weredetected, and sudden severe declines occurred over a fewmonths. These declines were asynchronous and spread as afront. Death of adults occurred as well as death of metamorphsat emergence, but the tadpoles survived. In two intensivelymonitored sites, mass mortality was seen at the time ofsignificant population declines (61, 74, 129). In these twolocations, diseased and dying frogs were found to be infectedwith chytrid fungi (7).

Examination of 272 wild and captive diseased frogs during anamphibian disease survey, between 1989 and 1999, revealedthat 54% were infected. In this study, chytrid infectionaccounted for almost all cases of unusual mortality in wild frogs(8). As a result of this study, the hypothesis was put forwardthat B. dendrobatidis was introduced into Australia in the 1970sin the Brisbane area, where the first dramatic declines occurred.The authors of the report also concluded that environmentaldegradation and immunosuppression did not appear to play arole in epidemics of chytridiomycosis. Many dead gravid frogsand dead frogs in good condition were found with chytridfungus infection.

Batrachochytrium is now widespread in frogs in Australia andhas so far been found in forty-four native myobatrachid andhylid species, in addition to cane toads (Bufo marinus) andaxolotyls (Ambystoma mexicanum). Infected frogs have beenfound in all states of Australia, except the Northern Territory. InWestern Australia, chytridiomycosis was detected in seventeenspecies, including both hylid and myobatrachid frogs (3).Between 1952 and 1984, 612 individuals were surveyed andfound to be negative. This supports the theory thatB. dendrobatidis is not a native pathogen of Western Australia.Estimates of annual mortality reach 50% in some anuranspecies. Although no species has yet suffered catastrophicdecline in south-western Australia, local extinctions haveoccurred.

Histological examination is useful for diagnosis of chytridinfection and may be used to survey toe clips from wild andcaptive amphibians, to survey archived specimens, to testanimals before translocation, and to determine the cause ofmortality in wild and captive anurans, thereby allowingappropriate management to be implemented. Using histology,

the chytrid fungus has been found in numerous species ofamphibians in Australia, the USA and Panama (9, 96). Mycotic dermatitis, reported as being caused byBasidiobolus ranarum infection, in Wyoming toads (Bufo baxteri)and Manitoba toads (Bufo hemiophrys) in the USA (123, 125)was probably actually due to Batrachochytrium infection.

Using light microscopy, sporangia can be observed in frog skinas walled round bodies (10 µm-30 µm diameter) insideepidermal cells (75). Details of sample collection, culture,pathology, disinfection and recognition of B. dendrobatidisinfection have been described in the literature (9, 75).

The chytrid fungus only invades the stratum corneum and thestratum granulosum (Fig. 3). Chytridiomycosis can bediagnosed using the routine haematoxylin and eosin stains.Special fungal stains, such as periodic acid-Schiff or silver stains(39) may be used, but do not appear to offer any additionalbenefit. Such stains may confirm infection in cases where a fewindistinct stages are present, or they may differentiate infectionof the epidermis by other fungi, for example cutaneousmucormycosis (124).


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E: epidermis

Fig. 3Section of skin from a heavily infected White’s tree frog (Litoriacaerulea)Note homogenous immature stage (I) of Batrachochytriumdendrobatidis, zoosporangium with discharge papillae (D) containingzoospores, and empty zoosporangium formed after zoospores havedischarged (arrow)

The chytrid fungus is associated with focal orthokeratotichyperkeratosis in the area of stratum corneum adjacent to theorganisms. In some fatal cases, an extensive sloughing of thehyperkeratotic layer may occur, leaving an epidermis with feworganisms. Healthy tadpoles may carry chytrids. The usualrange of fungal structures may be present in tadpole

Microscopy is highly sensitive for detecting chytrids in diseasedfrogs, but less sensitive for detecting subclinical infection inhealthy frogs. To produce simple, rapid and sensitive diagnostictests, panels of polyclonal and monoclonal antibodies havebeen generated (55) for use in ELISA andimmunohistochemistry. Freezing techniques have beendescribed whereby B. dendrobatidis can be frozen, stored andrecovered (55).

International movement of amphibians occurs primarily forcommerce or as deliberate or unintentional introductions, withsmaller numbers of animals moved in conservationprogrammes. Given that the chytrid fungus is susceptible todessication (L. Berger, personal communication), movement ofthe disease over long distances is most likely to have occurredvia movement of live amphibians. The magnitude of thesemovements is significant; for example, 180,000 amphibians ofat least twenty-one species from Europe listed in Appendices Iand II of the Berne Convention were imported into the UKbetween 1981 and 1990 (31).

Commercial activities centre on the pet, food and laboratoryanimal trades (P. Daszak and colleagues, personalcommunication; R. Mazzoni and colleagues, personalcommunication; 107). An example is farm-reared bullfrogs(Rana catesbeiana) which are transported internationally aseither live animals, or as frozen, skinned products. This tradesupports employment in the countries of origin, as well as inthe restaurants of Europe, Asia, North and South America, andelsewhere. Dwarf clawed frogs (Hymenochirus curtipes) of

African origin have been introduced widely throughout theUSA to stock ornamental ponds (33), and a wide range oftropical and temperate species are moved globally as part of thepet or amateur hobbyist trade. These trades are a particularconcern for disease introduction, since outdoor enclosuresallow contact between exotic and native species, and becauseexotic pet species are often released into inappropriate areasaccidentally or deliberately. Scientific use of amphibians hasalso created a commercial industry. For example, the laboratoryuse of African Xenopus species supports a significant movementof these species globally each year.

Deliberate international translocations of amphibians involveattempts at biocontrol, for example, the introduction of thecane toad into Australia, or release of exotic species into thewild for aesthetic reasons, for example, the release of exoticEuropean ranid frogs in the UK (7; P. Daszak and colleagues,personal communication). Unintentional national andinternational introductions also occur, such as the transport ofamphibians during movement of foodstuffs such as bananas.

Conservation programmes may also result in internationaltranslocation of amphibians (103). However, this movement ison a far smaller scale than commercial activities for the pet andfood trade, and disease testing and quarantine procedures areoften pre-requisites for translocation.

Consideration should be given to placing chytridiomycosis onthe Office International des Epizooties (OIE) List B, with theconsequent certification and testing requirements for importand export of amphibians (119). Guidelines on diseasescreening for amphibians in translocation programmes havebeen prepared by the Species Survival Commission VeterinarySpecialist Group of the World Conservation Union (IUCN)(32). This document includes recommendations for quarantineand testing for a variety of significant diseases of amphibians, inaddition to chytrid infection.

Treatment of clinical chytridiomycosis or amphibians possiblycarrying B. dendrobatidis has been described. The antimycoticdrug itraconazole has been used in baths (97) and administeredorally to treat affected adults (125). Benzalkonium chloride wasused to treat superficial mycotic dermatitis in dwarf clawedfrogs (46) which, based on microscopic lesions, was probablycaused by chytrid fungus. Treatment is costly and is only 80%effective in removing B. dendrobatidis from experimentallyinfected adults and tadpoles (R. Speare, personalcommunication).

Fomite transmission of B. dendrobatidis is also possible andequipment used to handle and hold amphibians should bewashed in water to remove any visible organic debris. Sodiumhypochlorite at 0.4%, or 70% ethanol for 1 min will killzoosporangia and zoospores. Drying for 3 h will killB. dendrobatidis.


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Fig. 4Section through mouthparts of a tadpole great barred frog(Mixophyes fasciolatus) with various stages ofBatrachochytrium dendrobatidis

mouthparts (Fig. 4). Tadpoles may have light infectionsaccompanied by minimal lesions, or heavier infections withhyperkeratosis.

Rabies as a model of emerging disease due tonatural or anthropogenic movement of animalsRabies is characterised by meningoencephalitis due to infectionof the central nervous system (CNS) by a lyssavirus (familyRhabdoviridae). When the CNS is affected, the disease is usuallyfatal, but long incubation or recovery are observed in somecases.

Rabies was originally described in dogs more than 2,500 yearsago (11). Rabies outbreaks have been reported in red foxes(Vulpes vulpes) since the 16th Century (12). In the NorthernHemisphere, large epizootics of rabies were reported in wildlifefrom the end of the 19th Century until early in the 20thCentury. Fox rabies in Europe is thought to have emerged alongthe border of Poland and Russia around the time of the SecondWorld War (106, 111). From this area, expansion of rabies hasbeen measured westward at 30 km-50 km annually (82, 128).The epizootic has primarily affected red foxes, with spillover toother mammals (132). By 1978, the areas affected by rabiesreached across Belgium, France, northern Italy and Austria, thegeographic expansion subsequently slowed for unexplainedreasons (12).

Around the world, rabies is characterised by large epizooticareas involving one or few reservoirs, such as the red fox inEurope. Molecular epidemiology has determined that a givenrabies virus strain is typically responsible for all affected animalsin a region (13). However, the situation can be more complexand new species can be involved. Racoon dogs (Nyctereutesprocyonoides), for example, were released in large numbers inRussia for the fur trade (40). The first racoon dogs wereobserved in Finland in the 1930s, but a population was wellestablished by the 1980s. Rabies reappeared in Finland in April1988, with racoon dogs being the primary species involved(100). Rabies was soon eradicated from Finland by oralvaccination, but is still a serious problem in Poland.

Two separate epidemiological forms of rabies exist in southernAfrica (127). Viverrids in general, and yellow mongoose(Cynictis penicillata) in particular, are affected by an ancientlineage of rabies virus. The other lineage affects domestic dogs,which are the major reservoir, and is responsible for spillover towild canids, with epizootics when the host population issufficiently large (95). This lineage may have been introducedfrom Europe into southern Africa in the late 1940s. Spilloversfrom one virus biotype into different hosts can occur but theinfluence of biotypes on the epizootiology of rabies in SouthernAfrica is not yet completely documented (131).

Rabies is a unique example of a persistent infection wherereservoir animals can be considered as both the principal victimand the vector of the disease. Based on work with African wilddogs (Lycaon pictus), Cleaveland and Dye (29) noted that thespecies which is responsible for maintaining rabies in an area isusually most susceptible to the homologous strain and excretes

the virus at high titre (10). This counter-intuitive adaptation ofthe virus to the principal host allows the infection to bemaintained among a community in which several species canbe sporadically affected but appear unable to sustain theinfection. Reservoir species are generally carnivores and mega-or micro-chiropterae (81). New hosts may be involved whendensity (i.e. contact rate allowing direct transmission) issufficient (133). Strains may emerge following passage withinthe new host species and become adapted; phylogeneticanalysis of the rabies virus strains from Europe revealed thatlocalised evolution, enabled by physical barriers and ecologicalconditions, has occurred. During recent evolution on thiscontinent, the rabies virus has made two species jumps; the firstfrom domestic dog to red fox, and more recently from fox toracoon dog (14). Observations from Europe and South Africasuggest that to survive in the long term in a new host, rabiesvirus probably requires a large population. Lethal strains ofrabies cannot sustain themselves in small isolated populations.Rabies can lead host populations close to extinction whenrecruitment is not sufficient to replenish the number ofsusceptible animals. In a large host population, such as the redfox in continental Europe, rabies is sustained by exchange ofthe virus among sub-populations (4). In this case, viralvirulence does not interfere with efficient transmission, but canlimit the reservoirs to relatively large species which are able tofrequently bite congeners. Other routes of transmission canfavour a less virulent lineage of virus if the reservoir is especiallygregarious, as observed in insectivorous or frugivorous bats.

Emergence of bat rabies over the previous decades in Europe,North America, and quite recently in Australia, appears to be adiscovery of an ancient infection rather than emergence of newvirus or contemporary adaptation of virus to new hosts. Ingeneral, mortality in rabies-infected bats appears to be low, withseroconversion occurring in many surviving individuals (81).Bats appear to be the preferred hosts of many lyssaviruses, andmany rabies viruses of terrestrial species may have originated inbats. Among the seven genotypes classically identified by crossimmunity and monoclonal antibody typing, more recentmolecular techniques have distinguished two phylogroups, thefirst encompassing classic rabies virus in terrestrial mammals(with several bat strains, including the Australian batlyssavirus); the second comprises Lagos bat and Mokola viruseswhich are less pathogenic (5), although fatalities have beenobserved in the USA and Australia.

The primary route of rabies virus transmission is through a bitewhich fails to induce strong humoral immunity. According toPeterhans et al. (104), this might be a strategy to avoid contactwith the immune system, the difference between virulent and‘mild’ strains being the ability of the virus to infect neuronsbefore a contact with immune cells. Thus, lethality is not amandatory adaptation in lyssavirus evolution. Most pathogensevolve towards less virulent strains, as described in 1964 byAndral who observed long asymptomatic incubation and somecases of recovery of dogs in Ethiopia from rabies virus


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infection (2). However, the maintenance of highly virulentstrains in a host population is possible.

Lyssavirus is an elusive and adaptable virus which survives inthe long term through the ability to cross species barriers ifecological conditions are favourable. Culling of foxes orextensive destruction of any rabies virus reservoir has neverbeen demonstrated to be effective in controlling rabies (12).Eradication was nevertheless achieved in Europe by oralimmunisation (122). This approach to control holds promise inother species in which oral vaccination is feasible. However,changes in ecological balance following rabies eradication maylead to game management and other public health problems(91). Risk of re-emergence of rabies following eradicationcannot be excluded because a high density of susceptible hostsis still present and various strains of lyssavirus are stillcirculating. Bat rabies can re-infect terrestrial hosts (81). Thus,countries which have controlled rabies first in domestic dogsand more recently in wildlife should not consider that thisdisease is a problem of the past. Such countries must look tothe future and maintain the ability to deal with rabies in thecoming years.

Changes in microbes or theirhost spectrum and technicalimprovements in epidemiologyNipah and Hendra virusesTwo paramyxoviruses from Australia, the Hendra virus andMenangle virus, have been described recently. Hendra viruswas first recognised in 1994 as a cause of acute, fatal disease inhorses and humans in two locations in Hendra and Mackay,Queensland, Australia (92, 93, 114). During the outbreak inHendra, 13 of 20 infected race horses died, as did a trainer andstablehand in contact with these horses. A second outbreak,approximately 1,000 km distant from Hendra, involved twofatalities in horses and one in a farmer. The two outbreaksappear unrelated, and no serological evidence of infection wasdetected in other domestic animal species, humans, or horses,thereby implicating a wildlife reservoir (109, 135, 141, 142).Natural Hendra virus infection was found to occur widely infour species of megachiropteran bats, the black (Pteropusalecto), grey-headed (P. poliocephalus), little red (P. scapulatus),and spectacled (P. conspicillatus) fruit bats. Interestingly, noserological evidence of infection has been found in people whotake care of large numbers of these and other species of bat(115). Serological evidence of Hendra virus infection has beenreported in six species of fruit bat (P. neohibernicus, Dobsoniamoluccensis, D. anderseni, P. capistratus, P. hypomelanus andP. admiralitatum) from Papua New Guinea (unpublished resultscited in 84). Although first classified as an equine morbillivirus,the host range, morphology, genome size, and coding for asmall basic protein, have led to proposed placement in a new

genus within the Paramyxoviridae (134, 143). Mackenzie (84)pointed out several unanswered questions regarding thebiological, ecological and pathological characteristics of Hendravirus, including the following:

– the apparent difficulty of interspecies transmission

– the proper classification of the virus

– the role of transmission during pregnancy

– the apparent latent period between infection and disease inhumans

– the transmission mechanisms between fruit bats and betweenbats and horses

– tissue tropisms in inapparent and acute infections.

The most important pathological manifestation of Hendra virusinfection in horses and humans is severe interstitial pneumonia(54). Diagnosis is based on isolation of the virus from blood,lung, kidney, spleen and brain tissue, and subsequentidentification.

Menangle virus was isolated from deformed new-born pigletsin New South Wales, Australia, in 1996. Infection resulted indecreased farrowing rates and numbers of piglets per litter andan increase in stillborn and mummified foetuses. Two workerswho had handled weaning pigs from this piggery had highMenangle antibody titres and a history of influenza-like viruswith rash. Large breeding colonies of grey-headed and little redfruit bats located near the affected piggery appeared to be thesource of the virus (105, 21).

Nipah virus spread among domestic pigs in Malaysia in 1998and 1999, causing a respiratory and neurological syndrome,sometimes accompanied by sudden death of adult animals. Thedisease in pigs has been termed porcine respiratory andneurological syndrome, porcine respiratory and encephalitissyndrome, or ‘barking pig’ syndrome (89). Nipah virus causedsevere encephalitis in humans who were in contact withinfected pigs on farms or in abattoirs. By mid-1999, more than265 cases of encephalitis and 105 deaths had been recorded inhumans, with 11 cases of encephalitis and 1 death reported inSingapore (27). Virus was isolated from a dog which hadcontact with infected pigs (19). In common with the Hendravirus, the Nipah virus is associated with pteropid fruit bats, thesuspected wildlife reservoir of this virus. Neutralising antibodywas found in five species of megachiropteran fruit bats(Cynopterus brachyotis, Eonycteris spelaea, Pteropus hypomelanusand P. vampyrus) and one insectivorous bat (Scotophilus kuhlii)(56). The means of Nipah virus transmission from bats to pigsis not known.

Nipah virus is related to, but distinguishable from Hendravirus, with 21% differences in nucleotide sequences and 8%differences in amino acid sequences (130). Diagnosis isestablished serologically by demonstration of IgG or by IgM


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capture in ELISAs (102) or by neutralisation tests with liveNipah virus in Vero cells tested by immunofluorescence withanti-Nipah virus monoclonal antibodies. Nipah virus can beisolated in vitro with syncytia or viral antigen demonstrated incell cultures. Fluorescent antibody tests andimmunohistochemistry may be used for diagnosis of infectionin animal tissues (19, 26). The virus can be visualised innegatively-stained preparations of cerebrospinal fluid bytransmission electron microscopy (25). Viral genomic materialcan be detected with RT-PCR (102). Control of the disease inpigs in Malaysia was accomplished by slaughter of swine oninfected premises, quarantine to stop movement of infectedanimals and implementation of a national surveillance andcontrol system to detect cases and cull infected herds (19).Human infection can be prevented by educating thoseindividuals at risk (farmers, abattoir workers, veterinarians)about avoiding direct contact with infected pigs and use ofprotective equipment (19). No measures are available to controlNipah virus in bats. Pigs should not be permitted to have accessto diseased or recently dead bats.

Tioman virus (TiV) was isolated from the urine of a fruit bat(P. hypomelanus) during a search for Nipah virus on an island offthe eastern coast of peninsular Malaysia (28). The onlyserological relationship between TiV and other knownparamyxoviruses is with Menangle virus found in Australia.The pathogenesis of TiV in other mammalian species isunknown.

Other examples of agents which have relatively recently crossedthe species barrier or broadened their host spectrum areencephalomyocarditis virus in free-ranging African elephant(45), and bovine tuberculosis in free-ranging lion (57).

ConclusionEmergence of infectious diseases in wildlife is a continuous andongoing process. The factors that give rise to these diseases,such as ecosystem alterations, movement of pathogens orvectors, and changes in pathogens may be natural or due tohuman influences. This chapter has reviewed some examples ofemerging diseases which illustrate these categories. The factorsthat result in emerging diseases are constantly acting on wildhosts and pathogens and these interactions can be expected tocontinue to result in new or newly recognised diseases in thefuture. Managers of wild species need to be cognisant of thefactors that give rise to emerging diseases and to be alert to theappearance of new diseases. This, of course, requiresknowledge of the endemic diseases in wild populations and theappropriate veterinary infrastructure to diagnose the spectrumof diseases in wildlife. Though intervention may not always beappropriate and will depend on many factors, in the case ofsome infectious diseases, managers of wildlife may need tointervene to protect populations or to prevent introduction orspread of emerging infectious diseases.


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Les maladies infectieuses émergentes de la faune sauvage

E.S. Williams, T. Yuill, M. Artois, J. Fischer & S.A. Haigh

RésuméLes facteurs à l’origine de l’émergence de maladies infectieuses affectant lafaune sauvage peuvent être rangés dans les catégories suivantes : altérationsnaturelles ou anthropogènes de l’écosystème ; déplacement d’agentspathogènes ou de vecteurs, par des moyens naturels ou artificiels ; mutationsmicrobiennes ou meilleure identification des agents pathogènes émergentsgrâce aux progrès des techniques épidémiologiques. Certes, cette classificationest un peu simpliste, car en réalité les facteurs favorisant l’émergence demaladies chez les animaux sauvages peuvent relever de plusieurs de cescatégories. La mycoplasmose des passereaux est associée à des modificationsde l’habitat et à l’alimentation artificielle, facteurs se traduisant par une plus forte

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densité des populations et donc par une capacité accrue de transmettre desmaladies. L’origine de la souche de Mycoplasma gallisepticum en cause n’estpas connue. Les infections dues aux hantavirus chez les rongeurs sont apparuesaprès l’altération du paysage par l’homme et/ou des changements climatiquesqui ont influencé la dynamique des populations d’hôtes réservoirs d’hantavirus,entraînant également un problème de santé publique. Le déplacement desagents pathogènes ou des vecteurs joue un rôle très important dans l’extensionde l’aire géographique des maladies de la faune sauvage. L’origine descalicivirus affectant le lapin et le lièvre n’est toujours pas élucidée, mais ledéplacement de ces animaux par l’homme, que ce soit délibérément ouaccidentellement, a beaucoup contribué à la diffusion de ces virus. La rage estune maladie ancienne, mais son expansion géographique a été favorisée par lesdéplacements naturels ou anthropogènes d’animaux sauvages. Lesdéplacements d’amphibiens par l’homme expliquent peut-être la répartitionmondiale de la chytridiale, un champignon très pathogène. La descriptionrécente des paramyxovirus reflète peut-être aussi bien une évolution de cesagents pathogènes que le développement des techniques de diagnostic et declassification. De nombreux autres exemples de maladies émergentes de ce typeapparaîtront à l’avenir, compte tenu de la modification à grande échelle despaysages dans le monde et des déplacements d’animaux, de vecteurs etd’agents pathogènes. Ceux qui étudient et diagnostiquent les maladies de lafaune sauvage doivent être vigilants à l’égard des maladies émergentes, afin deminimiser leur impact sur les espèces sauvages et domestiques, ainsi que surl’homme.

Mots-clésCalicivirus – Chytridiomycose – Faune sauvage – Hantavirus – Maladies émergentes –Mycoplasmose – Paramyxovirus – Rage.�

Enfermedades infecciosas emergentes de la fauna salvaje

E.S. Williams, T. Yuill, M. Artois, J. Fischer & S.A. Haigh

ResumenLos procesos que dan origen a enfermedades infecciosas de la fauna salvaje dereciente aparición pueden subdividirse en los siguientes: alteraciones de losecosistemas por causas naturales o antrópicas; desplazamiento de patógenos ovectores por medios naturales o artificiales; y cambios en los microorganismos oen las pautas de reconocimiento de nuevos patógenos debidos al avance de lastécnicas de epidemiología. Esta clasificación no deja de resultar algo burda, pueslos factores que influyen en la aparición de enfermedades de la fauna salvajesuelen corresponder a más de una de estas categorías. La micoplasmosis enaves paseriformes, por ejemplo, guarda relación no sólo con las alteraciones delhábitat sino también con la alimentación artificial, factores que inducen unamayor densidad de población que a su vez facilita la transmisión deenfermedades. Hoy por hoy se ignora el origen de la cepa de Mycoplasmagallisepticum responsable de la infección. Las infecciones de roedores porhantavirus, por su parte, obedecen a alteraciones del paisaje y/o cambiosclimáticos de origen antrópico que influyen en la dinámica de poblaciones de

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especies que ejercen de reservorio de hantavirus, lo que a la postre da lugar aprocesos infecciosos en el hombre. El movimiento de patógenos o vectores esuna de las principales causas de la ampliación del área de distribucióngeográfica de las enfermedades de la fauna salvaje. Aunque el origen de loscalicivirus que afectan a liebres y conejos sea hasta cierto punto una incógnita,se sabe que el desplazamiento de esos animales por el hombre, ya seadeliberada o accidentalmente, ha ampliado sobremanera el área de distribuciónde dichos virus. La rabia es una enfermedad antigua, pero se ha extendidogeográficamente a resultas del desplazamiento de animales salvajes por causastanto naturales como artificiales. El transporte de anfibios por el hombre puedeexplicar la distribución en todo el mundo del hongo quitridial altamentepatógeno. La reciente descripción de nuevos paramixovirus puede ser efectotanto de mutaciones sufridas por los patógenos como del desarrollo de lastécnicas de detección y clasificación. Considerando las profundas alteracionesde grandes extensiones naturales y el trasiego de animales, vectores ypatógenos que se vienen produciendo en todo el mundo, es de prever que en elfuturo sigan apareciendo muchos más ejemplos de este tipo. Los que se dedicanal estudio y diagnóstico de las patologías de la fauna salvaje deben extremar lavigilancia para detectar la aparición de enfermedades emergentes y minimizarasí sus consecuencias para los animales salvajes y domésticos, y el hombre.

Palabras claveCalicivirus – Fauna salvaje – Hantavirus – Micoplasmosis – Nuevas enfermedades –Paramixovirus – Quitridiomicosis – Rabia.

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