D528.PDF

Rev. sci. tech. Off. int. Epiz., 2002, 21 (1), 139-157
Emerging infectious diseases in 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, Wyoming
82070, United States of America
(2) Institute for Environmental Studies, University of Wisconsin, Madison, Wisconsin 53706, United States of
America
(3) Département de santé publique vétérinaire, Unité de pathologie infectieuse, École Nationale Vétérinaire de
Lyon, 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
Summary
The processes which give rise to emerging infectious diseases of wildlife can be
categorised as follows: ecosystem alterations of anthropogenic or natural origin;
movement of pathogens or vectors, via human or natural agency; and changes in
microbes or in the recognition of emerging pathogens due to advances in the
techniques of epidemiology. These are simplistic divisions because factors
influencing the emergence of diseases of wild animals generally fall into more
than one category. Mycoplasmosis among passerines is related to habitat
changes and artificial feeding resulting in increased bird densities and
subsequent disease transmission. The origin of this strain of Mycoplasma
gallisepticum is not known. Hantavirus infections in rodents have emerged due
to human-induced landscape alterations and/or climatic changes influencing
population dynamics of hantavirus reservoir hosts, with disease consequences
for humans. Movement of pathogens or vectors is a very important process by
which diseases of wildlife expand geographic range. Although the origin of
caliciviruses of rabbits and hares is somewhat obscure, their movement by
humans, either deliberately or accidentally, has greatly expanded the distribution
of these viruses. Rabies is an ancient disease, but geographic expansion has
occurred by both natural and anthropogenic movements of wild animals. Human
movement of amphibians may explain the distribution of the highly pathogenic
chytrid fungus around the world. Newly recognised paramyxoviruses may reflect
both changes in these pathogens and the development of techniques of
identification and classification. Many more such examples of emerging diseases
will arise in the future, given the extensive alterations in landscapes world-wide
and movements of animals, vectors and pathogens. Those who study and
diagnose diseases of wildlife must be alert for emerging diseases so that the
impact of such diseases on wild animals, domestic animals and humans can be
minimised.
Keywords
Caliciviruses – Chytridiomycosis – Emerging diseases – Hantaviruses – Mycoplasmosis –
Paramyxoviruses – Rabies – Wildlife.
Introduction
During the current period of increasing globalisation, the
emergence of new diseases of wildlife or the re-emergence of
old diseases should not be surprising (34). The world is
undergoing rapid ecological change, populated by pathogenic
organisms, their vectors and hosts which are capable of equally
rapid change. Some of these pathogens may cause significant
disease in wild species, but in other cases, the wild animals may
serve as reservoirs for pathogens which do not induce overt
illness in their wild hosts.
© OIE - 2002
140
Emerging infectious diseases have been defined by Morse (90)
as follows:
a) those diseases which have appeared in a population for the
first time, or
b) those diseases which have existed but are rapidly increasing
in prevalence or geographic range.
Although the term ‘emerging disease’ has been embraced by the
biomedical community and the media as a useful way to
categorise some diseases of humans and other animals, the term
is perhaps overused. ‘Emerging disease’ has become nearly
synonymous with epidemic or epizootic in the literature and in
grant applications. However, some categories of diseases
affecting or involving wild animals clearly meet the definition of
‘emerging’. This classification can assist in understanding these
diseases, in developing methods for control and management,
and in preventing the emergence of new diseases of wildlife.
Factors surrounding the emergence of infectious diseases of
wildlife fit into several categories. These have been best
described for human diseases (90), and have also been applied
to 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 natural
agency
c) changes in microbes or in the ability to recognise emerging
pathogens due to advances in the techniques of epidemiology.
Clearly, factors influencing emergence of many of the diseases
of wild animals fall into more than one category.
Alteration of ecosystems can create conditions which facilitate
the appearance and spread of new diseases. The duck plague
outbreak at Lake Andes, South Dakota, United States of
America (USA), is an example of the way in which
environmental management created conditions for the
outbreak of a new disease. Waterfowl managers kept lake water
open during the winter, which attracted large numbers of ducks
and geese. Duck plague virus, a herpesvirus which had been
recognised in the domestic duck industry in Long Island, New
York, USA, in 1967, unexpectedly appeared at Lake Andes in
1973 and rapidly killed over 43,000 ducks and geese (140).
Similarly, the creation of artificial water holes in Etosha National
Park, Namibia, created a situation resulting in repeated cases of
anthrax in large wild mammals (72).
Situations which favour disease appearance can also occur
inadvertently. Hardwood trees cut in south-western Wisconsin,
USA, form basal tree holes which collect water and increase the
numbers of breeding sites for Aedes triseriatus, the natural
mosquito vector of La Crosse virus. The reservoir of the virus is
small forest mammals. The virus is also transmitted to humans,
causing encephalitis, principally in pre-school age children
© OIE - 2002
Rev. sci. tech. Off. int. Epiz., 21 (1)
(126). Reforestation of the north-eastern USA favoured
transmission of Lyme borreliosis due to increased populations
of white-tailed deer (Odocoileus virginianus) and deer mice
(Peromyscus leucopus), and abundance of the tick vector, Ixodes
scapularis (17). In these cases, clinical disease is apparently not
a feature of infection of the wild animal host, but these animals
serve as reservoirs of the pathogens for domestic animals and
humans.
Natural climatic changes can increase host abundance and
transmission of pathogens, as in the case of Sin Nombre
hantavirus in the south-western USA. Increased rainfall
resulted in more grass setting seed and expansion of rodent
(Peromyscus spp.) populations which are natural reservoirs of
the virus, and thereby greater human contact with these mice
and their excretions (42). This resulted in virus transmission to
humans and the appearance of hantavirus pulmonary
syndrome (HPS). Although the virus was undoubtedly
endemic in rodent populations for centuries, causing sporadic
cases of human HPS, the aetiology was undiscovered until
1993 (112).
Movement of pathogens often occurs within animal hosts and
this can have significant impacts on naïve populations. The
interaction of wild and domestic species can result in serious
outbreaks of disease in wildlife. The epizootic of rinderpest in
Africa in the 1890s is one of the most dramatic examples of a
disease transmitted from domestic livestock to a virgin
population of wild ungulates, with resultant high mortality
(113). More recently, the appearance and rapid spread of
mycoplasmal conjunctivitis in wild songbirds raised questions
regarding the possible transmission of Mycoplasma gallisepticum
from backyard poultry to wild birds, although significant
antigenic differences between M. gallisepticum in wild birds and
isolates from commercial domestic poultry operations tend to
rule out that source of the epornitic (44).
Movement of pathogens has also accounted for the appearance
of wildlife diseases in new areas. Translocation of infected wild
and domestic animals has been an important factor in the
appearance of epizootics of rabies in new locations. Rabies
apparently was introduced into the New World by infected
dogs in the early 18th Century, with subsequent spillover into
a variety of wild terrestrial mammals. More recently, rabies
became established in racoons (Procyon lotor) in the midAtlantic states of the USA in the late 1970s, due to illegal
translocation of racoons into the region from the south-east
USA, where rabies was endemic in this species. Racoon rabies
continues to spread into the north-eastern (110) and midwestern USA. The domestic dog strain of rabies virus may have
been introduced from Europe to southern Africa, and hence
into wild canids.
However, the emergence of rabies across continental Europe
may have resulted in geographic expansion because of changes
in host populations, including numbers and species, but was
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probably not due to translocations. The surprising appearance
of disease due to West Nile virus in humans, horses, and wild
birds in New York, and the subsequent spread along the
Atlantic coast, is a very recent example of introduction and
establishment of a pathogen which apparently originated in the
Middle East. The mechanism of introduction into the USA is
unknown (20).
Although the origin of chronic wasting disease (CWD), a
spongiform encephalopathy of deer and elk, is not known,
movement of Rocky Mountain elk (Cervus elaphus nelsoni) in
the commercial game farm industry, has resulted in a greatly
expanded geographic distribution of CWD. The disease has
now been identified in privately-owned elk in six states of the
USA, in one province of Canada, and very recently, in the
Republic of Korea. The occurrence of CWD in the game farm
industry in Canada appears to have resulted in transmission of
the disease to free-ranging mule deer (Odocoileus hemionus) in
Saskatchewan, although this is still under study. A more
comprehensive discussion of CWD is provided in this issue of
the Review (139).
Movement of vectors can also contribute to the appearance of
diseases involving wildlife reservoirs. Ixodes scapularis, the
vector of Lyme borreliosis in North America, was found in the
upper Midwest for the first time in 1968. The tick has
subsequently spread in this region, probably due to transport
by wild birds (17).
Infectious diseases have been introduced deliberately into pest
wildlife populations as a means of population control. The
classical examples of the introduction of highly fatal viruses into
populations of an extremely susceptible host species are those
of myxomatosis and rabbit calicivirus into populations of
European rabbits (Oryctolagus cuniculus) in Australia (43, 68).
The contribution of exposure of wildlife to anthropogenic
effluents and toxicants to the appearance of new infectious and
parasitic diseases is not well understood. In 1993, an estimated
100,000 different chemicals were used annually world-wide
(94). The effects that these chemicals may have, alone or in
combination, on immune modulation and susceptibility to
infectious and parasitic diseases awaits further study. In
addition, these chemicals may cause alterations in habitats,
influencing animal and microbial numbers and distribution,
resulting in increasing impact of pathogens. Some examples
include possible association of agricultural run-off with blooms
of the dinoflagellate Phiesteria piscicida and disease in fish along
the southern Atlantic seaboard of the USA (18), and the serious
impact of Eustrongylides ignotus, a nematode parasite, on wading
birds in Florida, associated with alterations to the food chain
due to nutrient effluents in canals and ponds (116).
Mutation and recombination of pathogens can give rise to new
pathogens, or modification of existing ones. New pathogens
can arise through recombination. For example, the three
ribonucleic acid (RNA) segments of bunyaviruses such as La
Crosse and Jamestown Canyon can give rise to six distinct
reassortants in dually infected mosquitoes (23). The RNA is
subject to frequent mutations and there are no editing
mechanisms to repair the changes (63). Changes which appear
to be mutational may be phase variation in which genes such
as those that code for antigens, which have been part of the
genetic repertory, but silenced, are suddenly reactivated (63).
Activating and resilencing genes which code for antigens can
provide pathogenic parasites and bacteria with a mechanism to
escape the immunological defences of the host. Bacteria can
exchange genetic material through plasmid interchange, a well
recognised mechanism which permits the spread of antibiotic
resistance genes among widely differing species of bacteria.
As the powerful tools of molecular characterisation of
pathogens are improved, a better understanding of the
epidemiology of some of these agents is obtained. Application
of these techniques to pathogens such as Ehrlichia has revealed
the involvement of wild animals and humans. Thus, these
diseases may not be new, but their epidemiological stories are
now better appreciated (37).
The remainder of this review paper discusses some important
examples of emerging diseases of wildlife. The discussion is by
no means comprehensive because many other wildlife diseases
fit within the definitions of ‘emerging disease’. The intent is to
describe in greater detail a few wildlife diseases from around the
world which represent good examples of the factors associated
with disease ‘emergence’ in wild species.
Ecosystem alterations of
anthropogenic or natural origin
Mycoplasmal conjunctivitis of wild finches
Epornitic conjunctivitis in house finches (Carpodacus
mexicanus) was first reported in suburban Washington DC,
USA, during the winter of 1993-1994 when large numbers of
finches with swollen, crusty eyelids and nasal exudate were
observed at backyard feeding stations (Fig. 1). The vision of the
birds often was impaired and they were debilitated, reluctant to
leave feeding platforms, and easily captured by hand.
Mycoplasma gallisepticum was subsequently isolated from
conjunctival swabs of affected finches (69, 78). Although
antibodies against M. gallisepticum previously had been detected
in wild birds associated with poultry facilities in the USA (120),
M. gallisepticum had never been associated with clinical disease
in wild passerines. Mycoplasmal conjunctivitis was observed in
house finches in nine mid-Atlantic states by October 1994 and
throughout the entire eastern range of the species by 1996 (44).
To date, house finches with conjunctivitis have been reported
along the Atlantic coast from Quebec, Canada, to Florida and
westward from North Dakota to Texas.
House finches are sparrow-sized birds native to the western
USA. Capture and transport of finches from the western states
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Fig. 1
Extensive conjunctival inflammation, periorbital alopecia, and
nasal exudation in a house finch with Mycoplasma
gallisepticum infection
Fig. 2
Conjunctivitis in an American goldfinch with Mycoplasma
gallisepticum infection
for commercial sale in the eastern states occurred in the early
20th Century and the birds were introduced to Long Island,
New York, in about 1940 (41). House finches multiplied and
spread and now are common backyard birds throughout
eastern and mid-western North America. Although the eastern
house finch population now extends to the range of the western
population, mycoplasmal conjunctivitis has not been reported
in western house finches.
enhanced via direct contact, and an increased prevalence of
affected finches has been reported during this season (49).
Although precise modes of M. gallisepticum transmission among
wild finches are unknown, contamination of feeder surfaces
with M. gallisepticum has been documented and may serve as a
source of infection for finches (47). Additionally, eastern house
finches, unlike their western counterparts, may migrate several
hundreds of miles and could therefore disseminate a disease
agent over a large geographic area (6).
Since 1995, conjunctivitis due to M. gallisepticum infection has
been confirmed in other wild birds, including the American
goldfinch (Carduelis tristis) (Fig. 2) (44, 70), purple finch
(Carpodacus purpureus) (48), pine grosbeak (Pinicola
enucleator), and evening grosbeak (Coccothraustes vespertinus)
(87). Mycoplasmal conjunctivitis in goldfinches and a purple
finch has involved only a few scattered individuals suggesting
spillover from house finches. However, in early 1999, 10%20% of pine grosbeaks and evening grosbeaks at feeding
stations in north-eastern Quebec were affected by conjunctivitis
(87). Isolates of M. gallisepticum from house finches and other
affected species have been genetically indistinguishable,
suggesting that M. gallisepticum was transmitted from a single
source throughout wild bird populations. This strain of
M. gallisepticum differs from strains often associated with
mycoplasmal disease in domestic poultry as well as those used
in poultry vaccines. The origin of the finch M. gallisepticum
strain remains unknown (70).
The rapid spread of mycoplasmal conjunctivitis throughout the
range of the eastern house finch probably reflects both bird
behaviour and human activity (44). House finches are well
adapted to human land use practices and prefer to nest and
feed around buildings and farms as well as in suburban areas.
During the winter, house finches often flock to bird feeding
stations where transmission of infectious disease agents is
© OIE - 2002
Mycoplasma gallisepticum has long been recognised as a
significant pathogen of domestic poultry and farmed game
birds. The organism is the cause of chronic respiratory disease
in chickens and infectious sinusitis in turkeys (71). On rare
occasions, M. gallisepticum has caused infectious sinusitis in
wild turkeys closely associated with domestic poultry
operations (36). Keratoconjunctivitis due to infection with
M. gallisepticum has been reported in chickens (99) as well as in
farmed game birds such as pheasant (Phasianus colchicus) and
chukar partridge (Alectoris chukar) (30). The M. gallisepticum
strain of wild finches infected and elicited an antibody response
in domestic chickens and turkeys exposed to the organism
experimentally, but clinical disease was mild, if present at all
(101). In another experimental trial, M. gallisepticum was
transmitted from naturally-infected house finches to chickens,
but transmission required an extensive contact period (ten
weeks) and clinical disease was not apparent during the study
(121).
Conjunctivitis in wild birds may be detected via observation of
birds at backyard feeding stations and other sites. Indeed,
observation of birds at feeders was used successfully to
document the spread of mycoplasmal conjunctivitis via a
unique public survey known as the House Finch Disease
Survey of the Cornell Laboratory of Ornithology (38). The
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survey facilitated an investigation of disease trends across large
geographic areas which would have been impractical by
traditional means.
Diagnosis of mycoplasmal conjunctivitis can be confirmed only
by culture; however, clinical signs, gross and microscopic
lesions, serological testing, and molecular techniques can
provide a strong preliminary diagnosis. Gross lesions of
M. gallisepticum in house finches consist of unilateral or bilateral
conjunctival swelling with serous to mucoid ocular and nasal
discharge, crusts of dried exudate at the eyes and nares, and
periorbital alopecia due to self-trauma (79). Chronically and
severely affected birds may be thin. Microscopic lesions consist
of chronic inflammation of the ocular and upper respiratory
tissues (44, 79). Moderate to severe lymphoplasmacytic
inflammation, lymphoid hyperplasia, and epithelial hyperplasia
are present in the conjunctiva, and mild to moderate keratitis is
observed in some cases. Unilateral rhinitis is often present and
is characterised by mucosal necrosis, lymphoplasmacytic
inflammation, and hyperkeratosis of nasal turbinates. In fewer
cases, chronic, lymphoplasmacytic tracheitis is observed.
Transmission electron microscopy reveals adherent
mycoplasmal organisms on epithelial surfaces.
The serum plate agglutination (SPA) test is the serological assay
of choice for screening birds for M. gallisepticum antibodies
because it is simple, inexpensive, and can be used for many
avian species (58). The SPA test detects the earliest antibody
response produced and remains sensitive for a long period of
time; however, it has low specificity resulting in possible false
positives. Serological tests with higher specificity, such as the
haemagglutination inhibition test and enzyme-linked
immunosorbent assay (ELISA), should be used to confirm SPApositive samples (58). However, problems arise in applying
these tests to wild birds, due to difficulties in test interpretation
and disparities in reagents.
Polymerase chain reaction (PCR) techniques are sensitive and
timely alternatives to culture of M. gallisepticum. Specific
oligonucleotide primers are used to amplify small amounts of
nucleic acid to detectable levels (60). Random amplification of
polymorphic DNA (RAPD) or arbitrary primed PCR generate
DNA fingerprints which are used for molecular typing of strains
(70, 79). These techniques are valuable for molecular
epidemiological studies.
For culture of M. gallisepticum from affected birds, swabs of the
trachea, conjunctiva, choanal cleft, or infraorbital sinus are
placed into liquid growth media and incubated. Mycoplasma
gallisepticum is a fastidious organism which requires a complex
selective medium enriched with animal serum, dextrose, and a
yeast source. Frey’s medium with swine serum (FMS) is
frequently used (58). Other media used with success include
SP4 (138), PPLO (58), and Edward-type (15). Broth and agar
media are prepared with these formulations; penicillin and
thallium acetate may be added to inhibit growth of bacterial
and fungal contaminates. The broth is incubated until growth
is indicated, then plated on agar for identification procedures.
As with many diseases in free-ranging wildlife, mycoplasmal
conjunctivitis of wild birds is not easily treated or managed.
Individual birds may be captured and treated with
antimicrobial agents (136). However, this practice is of no
benefit to wildlife populations, and should therefore be
discouraged; chronically infected birds without clinical disease
may be released and serve as reservoirs of M. gallisepticum in the
wild, and M. gallisepticum has been transmitted from affected
house finches to other species in rehabilitation facilities (69).
Basic measures to lower potential disease risks at bird feeders
may reduce the transmission of mycoplasmosis in passerines
(77). Feeding stations should be cleaned and disinfected
regularly as well as spaced to reduce crowding. Only clean and
unspoiled feed should be used and spilled waste beneath
feeders should be cleaned up. If a local outbreak of
mycoplasmosis occurs, a temporary cessation of feeding may
help to disperse healthy birds before they become exposed. In
addition, physical contact between backyard domestic poultry
and wild birds should be prevented.
The ultimate impact of mycoplasmal conjunctivitis on wild bird
populations is uncertain. Since the beginning of the epornitic of
M. gallisepticum infection, house finch populations in several
eastern states have declined dramatically in areas where birds
occurred 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. gallisepticum
remains endemic in eastern house finches, but appears to have
declined in prevalence (49). Although several cases of clinical
conjunctivitis have been observed in goldfinches, purple
finches and house sparrows (Passer domesticus) in the eastern
USA, population declines have not been apparent in these
species (50). Other healthy wild birds have been positive for
M. gallisepticum antibodies, and tufted titmice (Baeolophus
bicolor) were positive by PCR, suggesting that this species may
be a subclinical carrier of M. gallisepticum or a closely related
mycoplasma (80).
Hantaviruses
Hantaviruses, members of the Bunyaviridae family, are found in
rodent reservoirs, and one insectivore, world-wide (Tables I, II
and III). Twenty-six distinct hantaviruses have been identified
(88). These viruses establish asymptomatic, persistent
infections in their rodent or insectivore hosts, but are the
aetiological agents of haemorrhagic fever with renal syndrome
of variable severity (83) in humans in Asia and Europe, and of
HPS in the Americas. Hantaan virus, the prototype of the
group, is the aetiological agent of Korean haemorrhagic fever
(64) and has caused thousands of cases annually in the People’s
Republic of China. The closely related Seoul virus causes milder
haemorrhagic disease and is distributed world-wide in the
Norway rat (Rattus norvegicus) through international
shipping (65).
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Table I
Hantaviruses causing haemorrhagic fever with renal syndrome
in humans (88)
Virus (a)
Hantaan
Known or suspected host Geographic distribution
(a)
Seoul
East Asia, Eastern Europe
East Asia, seaports
world-wide
Prospect Hill
Microtus pennsylvanicus
North America
Bloodland Lake
M. ochrogaster
North America
Balkans, Eastern Europe
Isla Vista
M. californicus
Western USA and Mexico
East Asia, Eastern Europe
El Moro Canyon
Reithrodontomys megalotis
Western USA and Mexico
Scandinavia, Europe,
Western Russia
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 Argentina
Clethrionomys glareolus
a) severe disease in humans
b) mild disease in humans
Table II
Hantaviruses causing hantavirus pulmonary syndrome in
humans (88)
Virus
Known or suspected host Geographic distribution
Sin Nombre
Peromyscus maniculatus
(grassland form)
West and Central USA
and Canada
New York
P. leucopus (eastern
haplotype)
Eastern USA
Black Creek Canal Sigmodon hispidus
(eastern form)
Florida
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
Hantavirus pulmonary syndrome was first recognised in the
south-western USA in 1993, and deer mice (Peromyscus
maniculatus) were demonstrated to be the reservoir (24).
Subsequently, other hantaviruses in a variety of rodents of the
Sigmodontinae family were shown to cause human HPS in the
Western Hemisphere. Precipitation, habitat structure, and food
availability are implicated as critical environmental factors
which affect rodent population dynamics as well as viral
transmission and persistence (1). Rodent hosts shed variable
amounts of these viruses in faeces, urine and saliva over long
periods of time. Infection in rodent hosts may persist despite
the presence of neutralising antibody. Bite wounds inflicted
during fighting appear to be a major mode of virus transmission
among rodents (88). Evidence exists for the direct human-tohuman transmission of one hantavirus, Andes virus, in
Argentina (137). Hantavirus infections are diagnosed by
serological methods (principally indirect fluorescent antibody,
enzyme immunoassay for immunoglobulin G [IgG] or IgM,
and a rapid strip immunoblot assay which can be used in the
field [52]), virus isolation, and demonstration of the presence
of virus by immunohistochemistry or of viral RNA by reverse
© OIE - 2002
Known or suspected host Geographic distribution
Rattus norvegicus
A. flavicollis (suspected)
Puumala
Virus
Apodemus agrarius
Dobrava/Belgrade Apodemus agrarius
(b)
Table III
Hantaviruses not known to cause disease in humans or
animals (88)
transcriptase PCR (RT-PCR) (59). Rodent control and
avoidance of contact with these reservoir hosts is the only
means to avoid infection of humans.
Movement of pathogens or
vectors via human or natural
agency
Calicivirus diseases of rabbits and hares
Rabbit haemorrhagic disease (RHD) has been variously termed
rabbit calicivirus disease, haemorrhagic tracheitis of rabbits,
haemorrhagic pneumonia of rabbits, necrotic hepatitis of
rabbits, rabbit plague, rabbit viral sudden death, and rabbit X
disease (68), reflecting the pathological characteristics and signs
of the disease. The disease first appeared in domestic rabbitries
in the People’s Republic of China in 1984, and later spread into
Europe, initially appearing in a severe epizootic in Italy in 1986,
in the United Kingdom (UK) in 1992, and then into North
Africa, spilling over from domestic rabbits to wild European
rabbits with significant mortality in both (86). The disease
appeared in domestic rabbits in Mexico in 1988, but was
rapidly eradicated (51).
After demonstrating that the RHD virus was specific for the
European rabbit host, the authorities responsible for rabbit
control in Australia conducted experiments in which rabbits
were exposed in large pens on Wardang Island (68). Although
these initial field trials on transmission of the virus among
penned rabbits did not appear promising, the virus escaped
from the island in 1995 and spread rapidly to disparate regions
of Australia, aided by deliberate introduction of the virus into
wild rabbit populations by farmers and pastoralists.
Unauthorised introduction of the disease into New Zealand
occurred in 1997. The virus spread directly among wild rabbits
or mechanically by arthropod vectors (67). Population
reductions of 65%-95% were recorded, and mortality has been
Rev. sci. tech. Off. int. Epiz., 21 (1)
highest where adult rabbits predominate over less susceptible
neonates and juveniles in the population. Case fatality
approaches 100% in susceptible adults. The few individuals
that do survive acquire lifelong immunity to subsequent
infection. Rabbit calicivirus disease has proved moderately
effective in controlling wild rabbits in Australia.
Sudden death of European rabbits in otherwise good bodily
condition suggests RHD. Definitive diagnosis is obtained by
demonstration of RHD virus antigen in spleen and liver cells by
immunohistochemistry or in tissue homogenates by ELISA,
human red cell haemagglutination, or demonstration of viral
RNA by PCR. Virus particles can be visualised by transmission
electron microscopy of liver homogenate supernatants.
Presence of RHD virus antibody can be demonstrated by ELISA
or inhibition of human red cell agglutination (22, 68). As the
virus does not replicate in vitro in cell cultures, inoculation of
susceptible rabbits is the best way to isolate infectious virus. No
effective measures have been found to control the disease in
wild rabbits. Translocation of individuals from areas where
epizootic RHD is occurring should be prevented if the objective
is to avoid spread of the disease.
European brown hare syndrome (EBHS), which is caused by a
virus related to RHD virus, has also been termed leporid
caliciviral hepatitis, viral hepatitis of hares, and acute hepatosis
(68). The disease, characterised by acute liver necrosis, caused
epizootics in European brown hares (Lepus europaeus). The
disease was first described in Sweden in the early 1980s, but
reports from the 1970s describe a disease with similar gross
lesions in European hares which died in England and other
countries of Europe, well before the appearance of RHD. Brown
and varying hares (Lepus timidus) are the only species shown to
be susceptible to this virus. Interestingly, European rabbits
inoculated with EBHS virus develop antibodies to the virus, but
not clinical disease. Similarly, European and varying hares
inoculated 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 develop
antibody. Comparison between RHD virus and EBHS virus
isolates has shown only 53%-71% homology between these
two groups. Comparison among isolates within the RHD virus
and EBHS virus groups has shown them to be 90% or more
homologous, indicating a distant relationship between, but not
within the groups (66, 98). Diagnosis of EBHS is essentially the
same as for RHD. In common with RHD virus, EBHS virus does
not replicate in cell cultures. Infected hares in nature may
exhibit abnormal behaviour and have been termed ‘crazy
hares’; the hares may lose fear of humans and dogs, and run in
circles (68). No effective measures are available to control EBHS
in populations of wild hares. Translocation of individuals from
foci of infection should be avoided.
Amphibian chytridiomycosis
‘Chytrid’ is the common name used for a phylum of fungi
characterised by asexual reproductive spores (zoospores) which
145
swim by means of a posteriorly directed flagellum (75). The
phylum currently contains a single class, five orders, and
approximately 120 genera. Based on the ultrastructure of the
zoospores and on sequences from the 18S ribosomal DNA
(rDNA), Batrachochytrium is classified in the largest order, the
Chytridiales. Batrachochytrium dendrobatidis is a fungus
belonging to this phylum and appears in two forms, namely: a
spherical sessile zoosporangium of 10 µm-40 µm in diameter,
and a motile zoospore of approximately 2 µm in diameter. The
motile zoospore attaches to the substrate, develops rhizoids,
and within four days becomes a zoosporangium. Zoospores are
then released as motile zoospores via discharge tubes.
Zoospores can live for over 24 h and are infective to frogs and
tadpoles
(L.
Berger,
personal
communication).
Batrachochytrium is the only genus of chytrid known to contain
a species which is pathogenic to vertebrates. Zoosporangia
grow only in the superficial keratinised layers of the epithelium.
In frogs, the fungus is most commonly found on the feet. In
tadpoles, B. dendrobatidis is found initially in the keratinised
mouthparts, and once these are lost, the organism invades the
newly keratinised tissues of the tail and feet.
Studies on ultrastructural morphology suggest that isolates
from the USA, Central America and Australia are closely related
(7, 76). Studies on sequences of the 18S rDNA of chytrids from
a wild White’s tree frog (Litoria caerulea) from Australia and a
poison dart frog (Dendrobates azureus) from America found
only five different base pairs of 1,700 sequenced (T.Y. James
and colleagues, personal communication). This adds support to
the hypothesis that B. dendrobatidis is a newly emerged agent.
In Australia, B. dendrobatidis has been found in frogs since 1989
and has been observed in the rainforests of southern, central
and northern Queensland and northern New South Wales. In
Queensland, Victoria, and Western Australia, chytridiomycosis
may have spread at approximately 100 km per year (3, 117,
118). The organism has been reported from anurans in
rainforests of Panama, in captive and wild frogs in the USA, and
in anurans which died at high altitudes in Ecuador. Evidence
has been found to suggest that B. dendrobatidis caused mass
mortality and population declines in high altitude, stream
dwelling rainforest anurans in protected areas of Queensland
and Panama (8).
The pattern of decline of many populations of frogs in Australia
is consistent with an epidemic after the suspected introduction
of B. dendrobatidis into numerous protected habitats after 1978.
Batrachochytrium was thought to be associated with sudden
declines in stream dwelling frogs even though tadpoles
survived. Tadpoles can carry infections in their mouthparts
from soon after hatching until metamorphic climax when the
beaks are shed and fungal sporangia are rapidly redistributed to
the skin of the body. Batrachochytrium may be able to avoid its
own extinction, as it moves into and decimates a population, by
subclinical infection of tadpoles and/or survival as a saprobe
(outside the amphibian host) (35). Healthy frogs also may be
© OIE - 2002
146
carriers of the fungus, and low levels of infection have been
found in clinically normal frogs from the wet tropics in
Queensland (R. Speare and M. Freeman, personal
communication).
Two potential causes of emergence of B. dendrobatidis as a
significant pathogen have been suggested, namely: introduction
into naïve populations and climate change. Several
characteristic features of the population declines of high
altitude, stream dwelling rainforest amphibians from protected
areas in Australia (85, 108) and Central America (73)
implicated a waterborne infectious disease: only stream
dwelling frogs disappeared, no environmental changes were
detected, and sudden severe declines occurred over a few
months. These declines were asynchronous and spread as a
front. Death of adults occurred as well as death of metamorphs
at emergence, but the tadpoles survived. In two intensively
monitored sites, mass mortality was seen at the time of
significant population declines (61, 74, 129). In these two
locations, diseased and dying frogs were found to be infected
with chytrid fungi (7).
Examination of 272 wild and captive diseased frogs during an
amphibian disease survey, between 1989 and 1999, revealed
that 54% were infected. In this study, chytrid infection
accounted for almost all cases of unusual mortality in wild frogs
(8). As a result of this study, the hypothesis was put forward
that B. dendrobatidis was introduced into Australia in the 1970s
in the Brisbane area, where the first dramatic declines occurred.
The authors of the report also concluded that environmental
degradation and immunosuppression did not appear to play a
role in epidemics of chytridiomycosis. Many dead gravid frogs
and dead frogs in good condition were found with chytrid
fungus infection.
Batrachochytrium is now widespread in frogs in Australia and
has so far been found in forty-four native myobatrachid and
hylid species, in addition to cane toads (Bufo marinus) and
axolotyls (Ambystoma mexicanum). Infected frogs have been
found in all states of Australia, except the Northern Territory. In
Western Australia, chytridiomycosis was detected in seventeen
species, including both hylid and myobatrachid frogs (3).
Between 1952 and 1984, 612 individuals were surveyed and
found to be negative. This supports the theory that
B. dendrobatidis is not a native pathogen of Western Australia.
Estimates of annual mortality reach 50% in some anuran
species. Although no species has yet suffered catastrophic
decline in south-western Australia, local extinctions have
occurred.
Histological examination is useful for diagnosis of chytrid
infection and may be used to survey toe clips from wild and
captive amphibians, to survey archived specimens, to test
animals before translocation, and to determine the cause of
mortality in wild and captive anurans, thereby allowing
appropriate management to be implemented. Using histology,
© OIE - 2002
Rev. sci. tech. Off. int. Epiz., 21 (1)
the chytrid fungus has been found in numerous species of
amphibians in Australia, the USA and Panama
(9, 96). Mycotic dermatitis, reported as being caused by
Basidiobolus 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 skin
as walled round bodies (10 µm-30 µm diameter) inside
epidermal cells (75). Details of sample collection, culture,
pathology, disinfection and recognition of B. dendrobatidis
infection have been described in the literature (9, 75).
The chytrid fungus only invades the stratum corneum and the
stratum granulosum (Fig. 3). Chytridiomycosis can be
diagnosed 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 additional
benefit. Such stains may confirm infection in cases where a few
indistinct stages are present, or they may differentiate infection
of the epidermis by other fungi, for example cutaneous
mucormycosis (124).
E: epidermis
Fig. 3
Section of skin from a heavily infected White’s tree frog (Litoria
caerulea)
Note homogenous immature stage (I) of Batrachochytrium
dendrobatidis, zoosporangium with discharge papillae (D) containing
zoospores, and empty zoosporangium formed after zoospores have
discharged (arrow)
The chytrid fungus is associated with focal orthokeratotic
hyperkeratosis in the area of stratum corneum adjacent to the
organisms. In some fatal cases, an extensive sloughing of the
hyperkeratotic layer may occur, leaving an epidermis with few
organisms. Healthy tadpoles may carry chytrids. The usual
range of fungal structures may be present in tadpole
Rev. sci. tech. Off. int. Epiz., 21 (1)
mouthparts (Fig. 4). Tadpoles may have light infections
accompanied by minimal lesions, or heavier infections with
hyperkeratosis.
147
African origin have been introduced widely throughout the
USA to stock ornamental ponds (33), and a wide range of
tropical and temperate species are moved globally as part of the
pet or amateur hobbyist trade. These trades are a particular
concern for disease introduction, since outdoor enclosures
allow contact between exotic and native species, and because
exotic pet species are often released into inappropriate areas
accidentally or deliberately. Scientific use of amphibians has
also created a commercial industry. For example, the laboratory
use of African Xenopus species supports a significant movement
of these species globally each year.
Deliberate international translocations of amphibians involve
attempts at biocontrol, for example, the introduction of the
cane toad into Australia, or release of exotic species into the
wild for aesthetic reasons, for example, the release of exotic
European ranid frogs in the UK (7; P. Daszak and colleagues,
personal communication). Unintentional national and
international introductions also occur, such as the transport of
amphibians during movement of foodstuffs such as bananas.
Fig. 4
Section through mouthparts of a tadpole great barred frog
(Mixophyes fasciolatus) with various stages of
Batrachochytrium dendrobatidis
Microscopy is highly sensitive for detecting chytrids in diseased
frogs, but less sensitive for detecting subclinical infection in
healthy frogs. To produce simple, rapid and sensitive diagnostic
tests, panels of polyclonal and monoclonal antibodies have
been generated (55) for use in ELISA and
immunohistochemistry. Freezing techniques have been
described whereby B. dendrobatidis can be frozen, stored and
recovered (55).
International movement of amphibians occurs primarily for
commerce or as deliberate or unintentional introductions, with
smaller numbers of animals moved in conservation
programmes. Given that the chytrid fungus is susceptible to
dessication (L. Berger, personal communication), movement of
the disease over long distances is most likely to have occurred
via movement of live amphibians. The magnitude of these
movements is significant; for example, 180,000 amphibians of
at least twenty-one species from Europe listed in Appendices I
and II of the Berne Convention were imported into the UK
between 1981 and 1990 (31).
Commercial activities centre on the pet, food and laboratory
animal trades (P. Daszak and colleagues, personal
communication; R. Mazzoni and colleagues, personal
communication; 107). An example is farm-reared bullfrogs
(Rana catesbeiana) which are transported internationally as
either live animals, or as frozen, skinned products. This trade
supports employment in the countries of origin, as well as in
the restaurants of Europe, Asia, North and South America, and
elsewhere. Dwarf clawed frogs (Hymenochirus curtipes) of
Conservation programmes may also result in international
translocation of amphibians (103). However, this movement is
on a far smaller scale than commercial activities for the pet and
food trade, and disease testing and quarantine procedures are
often pre-requisites for translocation.
Consideration should be given to placing chytridiomycosis on
the Office International des Epizooties (OIE) List B, with the
consequent certification and testing requirements for import
and export of amphibians (119). Guidelines on disease
screening for amphibians in translocation programmes have
been prepared by the Species Survival Commission Veterinary
Specialist Group of the World Conservation Union (IUCN)
(32). This document includes recommendations for quarantine
and testing for a variety of significant diseases of amphibians, in
addition to chytrid infection.
Treatment of clinical chytridiomycosis or amphibians possibly
carrying B. dendrobatidis has been described. The antimycotic
drug itraconazole has been used in baths (97) and administered
orally to treat affected adults (125). Benzalkonium chloride was
used to treat superficial mycotic dermatitis in dwarf clawed
frogs (46) which, based on microscopic lesions, was probably
caused by chytrid fungus. Treatment is costly and is only 80%
effective in removing B. dendrobatidis from experimentally
infected adults and tadpoles (R. Speare, personal
communication).
Fomite transmission of B. dendrobatidis is also possible and
equipment used to handle and hold amphibians should be
washed in water to remove any visible organic debris. Sodium
hypochlorite at 0.4%, or 70% ethanol for 1 min will kill
zoosporangia and zoospores. Drying for 3 h will kill
B. dendrobatidis.
© OIE - 2002
148
Rabies as a model of emerging disease due to
natural or anthropogenic movement of animals
Rabies is characterised by meningoencephalitis due to infection
of the central nervous system (CNS) by a lyssavirus (family
Rhabdoviridae). When the CNS is affected, the disease is usually
fatal, but long incubation or recovery are observed in some
cases.
Rabies was originally described in dogs more than 2,500 years
ago (11). Rabies outbreaks have been reported in red foxes
(Vulpes vulpes) since the 16th Century (12). In the Northern
Hemisphere, large epizootics of rabies were reported in wildlife
from the end of the 19th Century until early in the 20th
Century. Fox rabies in Europe is thought to have emerged along
the border of Poland and Russia around the time of the Second
World War (106, 111). From this area, expansion of rabies has
been measured westward at 30 km-50 km annually (82, 128).
The epizootic has primarily affected red foxes, with spillover to
other mammals (132). By 1978, the areas affected by rabies
reached across Belgium, France, northern Italy and Austria, the
geographic expansion subsequently slowed for unexplained
reasons (12).
Around the world, rabies is characterised by large epizootic
areas involving one or few reservoirs, such as the red fox in
Europe. Molecular epidemiology has determined that a given
rabies virus strain is typically responsible for all affected animals
in a region (13). However, the situation can be more complex
and new species can be involved. Racoon dogs (Nyctereutes
procyonoides), for example, were released in large numbers in
Russia for the fur trade (40). The first racoon dogs were
observed in Finland in the 1930s, but a population was well
established by the 1980s. Rabies reappeared in Finland in April
1988, with racoon dogs being the primary species involved
(100). Rabies was soon eradicated from Finland by oral
vaccination, but is still a serious problem in Poland.
Two separate epidemiological forms of rabies exist in southern
Africa (127). Viverrids in general, and yellow mongoose
(Cynictis penicillata) in particular, are affected by an ancient
lineage of rabies virus. The other lineage affects domestic dogs,
which are the major reservoir, and is responsible for spillover to
wild canids, with epizootics when the host population is
sufficiently large (95). This lineage may have been introduced
from Europe into southern Africa in the late 1940s. Spillovers
from one virus biotype into different hosts can occur but the
influence of biotypes on the epizootiology of rabies in Southern
Africa is not yet completely documented (131).
Rabies is a unique example of a persistent infection where
reservoir animals can be considered as both the principal victim
and the vector of the disease. Based on work with African wild
dogs (Lycaon pictus), Cleaveland and Dye (29) noted that the
species which is responsible for maintaining rabies in an area is
usually most susceptible to the homologous strain and excretes
© OIE - 2002
Rev. sci. tech. Off. int. Epiz., 21 (1)
the virus at high titre (10). This counter-intuitive adaptation of
the virus to the principal host allows the infection to be
maintained among a community in which several species can
be sporadically affected but appear unable to sustain the
infection. Reservoir species are generally carnivores and megaor micro-chiropterae (81). New hosts may be involved when
density (i.e. contact rate allowing direct transmission) is
sufficient (133). Strains may emerge following passage within
the new host species and become adapted; phylogenetic
analysis of the rabies virus strains from Europe revealed that
localised evolution, enabled by physical barriers and ecological
conditions, has occurred. During recent evolution on this
continent, the rabies virus has made two species jumps; the first
from domestic dog to red fox, and more recently from fox to
racoon dog (14). Observations from Europe and South Africa
suggest that to survive in the long term in a new host, rabies
virus probably requires a large population. Lethal strains of
rabies cannot sustain themselves in small isolated populations.
Rabies can lead host populations close to extinction when
recruitment is not sufficient to replenish the number of
susceptible animals. In a large host population, such as the red
fox in continental Europe, rabies is sustained by exchange of
the virus among sub-populations (4). In this case, viral
virulence does not interfere with efficient transmission, but can
limit the reservoirs to relatively large species which are able to
frequently bite congeners. Other routes of transmission can
favour a less virulent lineage of virus if the reservoir is especially
gregarious, 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 a
discovery of an ancient infection rather than emergence of new
virus or contemporary adaptation of virus to new hosts. In
general, mortality in rabies-infected bats appears to be low, with
seroconversion occurring in many surviving individuals (81).
Bats appear to be the preferred hosts of many lyssaviruses, and
many rabies viruses of terrestrial species may have originated in
bats. Among the seven genotypes classically identified by cross
immunity and monoclonal antibody typing, more recent
molecular techniques have distinguished two phylogroups, the
first encompassing classic rabies virus in terrestrial mammals
(with several bat strains, including the Australian bat
lyssavirus); the second comprises Lagos bat and Mokola viruses
which are less pathogenic (5), although fatalities have been
observed in the USA and Australia.
The primary route of rabies virus transmission is through a bite
which fails to induce strong humoral immunity. According to
Peterhans et al. (104), this might be a strategy to avoid contact
with the immune system, the difference between virulent and
‘mild’ strains being the ability of the virus to infect neurons
before a contact with immune cells. Thus, lethality is not a
mandatory adaptation in lyssavirus evolution. Most pathogens
evolve towards less virulent strains, as described in 1964 by
Andral who observed long asymptomatic incubation and some
cases of recovery of dogs in Ethiopia from rabies virus
149
Rev. sci. tech. Off. int. Epiz., 21 (1)
infection (2). However, the maintenance of highly virulent
strains in a host population is possible.
Lyssavirus is an elusive and adaptable virus which survives in
the long term through the ability to cross species barriers if
ecological conditions are favourable. Culling of foxes or
extensive destruction of any rabies virus reservoir has never
been demonstrated to be effective in controlling rabies (12).
Eradication was nevertheless achieved in Europe by oral
immunisation (122). This approach to control holds promise in
other species in which oral vaccination is feasible. However,
changes in ecological balance following rabies eradication may
lead to game management and other public health problems
(91). Risk of re-emergence of rabies following eradication
cannot be excluded because a high density of susceptible hosts
is still present and various strains of lyssavirus are still
circulating. Bat rabies can re-infect terrestrial hosts (81). Thus,
countries which have controlled rabies first in domestic dogs
and more recently in wildlife should not consider that this
disease is a problem of the past. Such countries must look to
the future and maintain the ability to deal with rabies in the
coming years.
Changes in microbes or their
host spectrum and technical
improvements in epidemiology
Nipah and Hendra viruses
Two paramyxoviruses from Australia, the Hendra virus and
Menangle virus, have been described recently. Hendra virus
was first recognised in 1994 as a cause of acute, fatal disease in
horses and humans in two locations in Hendra and Mackay,
Queensland, Australia (92, 93, 114). During the outbreak in
Hendra, 13 of 20 infected race horses died, as did a trainer and
stablehand in contact with these horses. A second outbreak,
approximately 1,000 km distant from Hendra, involved two
fatalities in horses and one in a farmer. The two outbreaks
appear unrelated, and no serological evidence of infection was
detected 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 in
four species of megachiropteran bats, the black (Pteropus
alecto), grey-headed (P. poliocephalus), little red (P. scapulatus),
and spectacled (P. conspicillatus) fruit bats. Interestingly, no
serological evidence of infection has been found in people who
take care of large numbers of these and other species of bat
(115). Serological evidence of Hendra virus infection has been
reported in six species of fruit bat (P. neohibernicus, Dobsonia
moluccensis, D. anderseni, P. capistratus, P. hypomelanus and
P. admiralitatum) from Papua New Guinea (unpublished results
cited in 84). Although first classified as an equine morbillivirus,
the host range, morphology, genome size, and coding for a
small basic protein, have led to proposed placement in a new
genus within the Paramyxoviridae (134, 143). Mackenzie (84)
pointed out several unanswered questions regarding the
biological, ecological and pathological characteristics of Hendra
virus, 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 in
humans
– the transmission mechanisms between fruit bats and between
bats and horses
– tissue tropisms in inapparent and acute infections.
The most important pathological manifestation of Hendra virus
infection 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 subsequent
identification.
Menangle virus was isolated from deformed new-born piglets
in New South Wales, Australia, in 1996. Infection resulted in
decreased farrowing rates and numbers of piglets per litter and
an increase in stillborn and mummified foetuses. Two workers
who had handled weaning pigs from this piggery had high
Menangle antibody titres and a history of influenza-like virus
with rash. Large breeding colonies of grey-headed and little red
fruit bats located near the affected piggery appeared to be the
source of the virus (105, 21).
Nipah virus spread among domestic pigs in Malaysia in 1998
and 1999, causing a respiratory and neurological syndrome,
sometimes accompanied by sudden death of adult animals. The
disease in pigs has been termed porcine respiratory and
neurological syndrome, porcine respiratory and encephalitis
syndrome, or ‘barking pig’ syndrome (89). Nipah virus caused
severe encephalitis in humans who were in contact with
infected pigs on farms or in abattoirs. By mid-1999, more than
265 cases of encephalitis and 105 deaths had been recorded in
humans, with 11 cases of encephalitis and 1 death reported in
Singapore (27). Virus was isolated from a dog which had
contact with infected pigs (19). In common with the Hendra
virus, the Nipah virus is associated with pteropid fruit bats, the
suspected wildlife reservoir of this virus. Neutralising antibody
was found in five species of megachiropteran fruit bats
(Cynopterus brachyotis, Eonycteris spelaea, Pteropus hypomelanus
and P. vampyrus) and one insectivorous bat (Scotophilus kuhlii)
(56). The means of Nipah virus transmission from bats to pigs
is not known.
Nipah virus is related to, but distinguishable from Hendra
virus, with 21% differences in nucleotide sequences and 8%
differences in amino acid sequences (130). Diagnosis is
established serologically by demonstration of IgG or by IgM
© OIE - 2002
150
Rev. sci. tech. Off. int. Epiz., 21 (1)
capture in ELISAs (102) or by neutralisation tests with live
Nipah virus in Vero cells tested by immunofluorescence with
anti-Nipah virus monoclonal antibodies. Nipah virus can be
isolated in vitro with syncytia or viral antigen demonstrated in
cell
cultures.
Fluorescent
antibody
tests
and
immunohistochemistry may be used for diagnosis of infection
in animal tissues (19, 26). The virus can be visualised in
negatively-stained preparations of cerebrospinal fluid by
transmission electron microscopy (25). Viral genomic material
can be detected with RT-PCR (102). Control of the disease in
pigs in Malaysia was accomplished by slaughter of swine on
infected premises, quarantine to stop movement of infected
animals and implementation of a national surveillance and
control system to detect cases and cull infected herds (19).
Human infection can be prevented by educating those
individuals at risk (farmers, abattoir workers, veterinarians)
about avoiding direct contact with infected pigs and use of
protective equipment (19). No measures are available to control
Nipah virus in bats. Pigs should not be permitted to have access
to 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 off
the eastern coast of peninsular Malaysia (28). The only
serological relationship between TiV and other known
paramyxoviruses is with Menangle virus found in Australia.
The pathogenesis of TiV in other mammalian species is
unknown.
Conclusion
Emergence of infectious diseases in wildlife is a continuous and
ongoing process. The factors that give rise to these diseases,
such as ecosystem alterations, movement of pathogens or
vectors, and changes in pathogens may be natural or due to
human influences. This chapter has reviewed some examples of
emerging diseases which illustrate these categories. The factors
that result in emerging diseases are constantly acting on wild
hosts and pathogens and these interactions can be expected to
continue to result in new or newly recognised diseases in the
future. Managers of wild species need to be cognisant of the
factors that give rise to emerging diseases and to be alert to the
appearance of new diseases. This, of course, requires
knowledge of the endemic diseases in wild populations and the
appropriate veterinary infrastructure to diagnose the spectrum
of diseases in wildlife. Though intervention may not always be
appropriate and will depend on many factors, in the case of
some infectious diseases, managers of wildlife may need to
intervene to protect populations or to prevent introduction or
spread of emerging infectious diseases.
Other examples of agents which have relatively recently crossed
the species barrier or broadened their host spectrum are
encephalomyocarditis virus in free-ranging African elephant
(45), and bovine tuberculosis in free-ranging lion (57).
■
Les maladies infectieuses émergentes de la faune sauvage
E.S. Williams, T. Yuill, M. Artois, J. Fischer & S.A. Haigh
Résumé
Les facteurs à l’origine de l’émergence de maladies infectieuses affectant la
faune sauvage peuvent être rangés dans les catégories suivantes : altérations
naturelles ou anthropogènes de l’écosystème ; déplacement d’agents
pathogènes ou de vecteurs, par des moyens naturels ou artificiels ; mutations
microbiennes ou meilleure identification des agents pathogènes émergents
grâce aux progrès des techniques épidémiologiques. Certes, cette classification
est un peu simpliste, car en réalité les facteurs favorisant l’émergence de
maladies chez les animaux sauvages peuvent relever de plusieurs de ces
catégories. La mycoplasmose des passereaux est associée à des modifications
de l’habitat et à l’alimentation artificielle, facteurs se traduisant par une plus forte
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Rev. sci. tech. Off. int. Epiz., 21 (1)
densité des populations et donc par une capacité accrue de transmettre des
maladies. L’origine de la souche de Mycoplasma gallisepticum en cause n’est
pas connue. Les infections dues aux hantavirus chez les rongeurs sont apparues
après l’altération du paysage par l’homme et/ou des changements climatiques
qui ont influencé la dynamique des populations d’hôtes réservoirs d’hantavirus,
entraînant également un problème de santé publique. Le déplacement des
agents pathogènes ou des vecteurs joue un rôle très important dans l’extension
de l’aire géographique des maladies de la faune sauvage. L’origine des
calicivirus affectant le lapin et le lièvre n’est toujours pas élucidée, mais le
déplacement de ces animaux par l’homme, que ce soit délibérément ou
accidentellement, a beaucoup contribué à la diffusion de ces virus. La rage est
une maladie ancienne, mais son expansion géographique a été favorisée par les
déplacements naturels ou anthropogènes d’animaux sauvages. Les
déplacements d’amphibiens par l’homme expliquent peut-être la répartition
mondiale de la chytridiale, un champignon très pathogène. La description
récente des paramyxovirus reflète peut-être aussi bien une évolution de ces
agents pathogènes que le développement des techniques de diagnostic et de
classification. De nombreux autres exemples de maladies émergentes de ce type
apparaîtront à l’avenir, compte tenu de la modification à grande échelle des
paysages dans le monde et des déplacements d’animaux, de vecteurs et
d’agents pathogènes. Ceux qui étudient et diagnostiquent les maladies de la
faune sauvage doivent être vigilants à l’égard des maladies émergentes, afin de
minimiser leur impact sur les espèces sauvages et domestiques, ainsi que sur
l’homme.
Mots-clés
Calicivirus – 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
Resumen
Los procesos que dan origen a enfermedades infecciosas de la fauna salvaje de
reciente aparición pueden subdividirse en los siguientes: alteraciones de los
ecosistemas por causas naturales o antrópicas; desplazamiento de patógenos o
vectores por medios naturales o artificiales; y cambios en los microorganismos o
en las pautas de reconocimiento de nuevos patógenos debidos al avance de las
técnicas de epidemiología. Esta clasificación no deja de resultar algo burda, pues
los factores que influyen en la aparición de enfermedades de la fauna salvaje
suelen corresponder a más de una de estas categorías. La micoplasmosis en
aves paseriformes, por ejemplo, guarda relación no sólo con las alteraciones del
hábitat sino también con la alimentación artificial, factores que inducen una
mayor densidad de población que a su vez facilita la transmisión de
enfermedades. Hoy por hoy se ignora el origen de la cepa de Mycoplasma
gallisepticum responsable de la infección. Las infecciones de roedores por
hantavirus, por su parte, obedecen a alteraciones del paisaje y/o cambios
climáticos de origen antrópico que influyen en la dinámica de poblaciones de
© OIE - 2002
152
Rev. sci. tech. Off. int. Epiz., 21 (1)
especies que ejercen de reservorio de hantavirus, lo que a la postre da lugar a
procesos infecciosos en el hombre. El movimiento de patógenos o vectores es
una de las principales causas de la ampliación del área de distribución
geográfica de las enfermedades de la fauna salvaje. Aunque el origen de los
calicivirus que afectan a liebres y conejos sea hasta cierto punto una incógnita,
se sabe que el desplazamiento de esos animales por el hombre, ya sea
deliberada o accidentalmente, ha ampliado sobremanera el área de distribución
de dichos virus. La rabia es una enfermedad antigua, pero se ha extendido
geográficamente a resultas del desplazamiento de animales salvajes por causas
tanto naturales como artificiales. El transporte de anfibios por el hombre puede
explicar la distribución en todo el mundo del hongo quitridial altamente
patógeno. La reciente descripción de nuevos paramixovirus puede ser efecto
tanto de mutaciones sufridas por los patógenos como del desarrollo de las
técnicas de detección y clasificación. Considerando las profundas alteraciones
de grandes extensiones naturales y el trasiego de animales, vectores y
patógenos que se vienen produciendo en todo el mundo, es de prever que en el
futuro sigan apareciendo muchos más ejemplos de este tipo. Los que se dedican
al estudio y diagnóstico de las patologías de la fauna salvaje deben extremar la
vigilancia para detectar la aparición de enfermedades emergentes y minimizar
así sus consecuencias para los animales salvajes y domésticos, y el hombre.
Palabras clave
Calicivirus – Fauna salvaje – Hantavirus – Micoplasmosis – Nuevas enfermedades –
Paramixovirus – Quitridiomicosis – Rabia.
■
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