D9029.PDF

Rev. sci. tech. Off. int. Epiz., 1996, 15 (1), 9 1 - 1 1 4
Infectious and parasitic diseases of captive
carnivores, with special emphasis on the
black-footed ferret (Mustela nigripes)
E.S. WILLIAMS * and E.T. THORNE **
Summary: Captive carnivores are susceptible to a wide array of infectious
and parasitic diseases, which reflects the diversity of the seven families of
Carnivora. Unfortunately, relatively few in-depth studies have been conducted
on diseases of non-domestic carnivores, and much remains to be learned,
especially regarding diseases of small carnivores (e.g. mustelids, viverrids and
procyonids). The more important infectious diseases of carnivores include
rabies, canine distemper, and diseases caused by parvoviruses, coronaviruses
and herpesviruses. Few parasitic or bacterial pathogens are significant in
captive populations, and appropriate husbandry, therapy, vaccines and
quarantine minimize the risk of disease. Extrapolations from one species to
another regarding disease susceptibility may be incorrect. The black-footed
ferret (Mustela nigripes) serves as an example of a carnivore significantly
affected by infectious diseases, some of which were expected while others
could not have been predicted from generalized knowledge of diseases of
mustelids. This highlights the need to understand the natural history of each
species maintained in captivity.
KEYWORDS: Black-footed ferret - Canidae - Carnivora - Felidae Hyaenidae - Infectious diseases - Mustela nigripes - Mustelidae Procyonidae — Ursidae — Viverridae.
INTRODUCTION
The order Carnivora encompasses an extremely varied group of species which are
hosts to a correspondingly diverse spectrum of infectious agents. The order is
composed of seven extant families (98), namely Canidae (dogs, wolves, coyotes,
jackals, foxes), Felidae (cats), Mustelidae (weasels, badgers, skunks and otters),
Ursidae (bears, giant panda), Procyonidae (raccoons and relatives, lesser pandas),
Viverridae (civets, genets, linsangs, mongooses, fossas) and Hyaenidae (hyenas,
aardwolf). Non-domesticated carnivores are held in captivity for educational and
recreational purposes, for fur production, as pets, for research, in captive breeding
programmes for endangered species recovery and species conservation, and for
rehabilitation. Some individuals are generations removed from the free-ranging state
* Department of Veterinary Sciences, University of Wyoming, Laramie, Wyoming 82070, United
States of America.
** Wyoming Game and Fish Department, Box 3312, University Station, Laramie, Wyoming 82071,
United States of America.
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but are still considered 'wild' because they are not truly domesticated (33); others may
have been removed from the wild only recently. The burden of infectious diseases and
parasites is influenced by many factors, including the length of time since the animals
were removed from the wild, degree of adjustment to captivity, quality of captive
management and husbandry for the needs of the species, and proximity to other
species with which they could exchange pathogens. Sources of infectious agents for
captive carnivores are varied, and include contact with the following:
- individuals of the same, related or distant species
- humans
-
food
- water
-
fomites
- iatrogenic introduction, e.g. through attenuated vaccines.
Carnivores display a spectrum of disease susceptibility, and understanding of the
diseases of many species is incomplete at present.
In this review, the disease situation of the carnivores is organized according to
family, and the most significant infectious and parasitic diseases of each group are
discussed. Diseases were chosen by reason of their impact on species, or their
importance to the health of humans, domestic animals, and captive or free-ranging
animals; these diseases are therefore of concern to those maintaining and exchanging
carnivores in captivity. Following this section is a review of the recovery programme
for the black-footed ferret (Mustela nigripes), as an example of a captive endangered
wild species which is significantly affected by infectious diseases. General lists of
infectious diseases of various families may contrast sharply with the specific disease
problems of one species. This highlights the need to understand the range of disease
susceptibility in specific species of interest, and emphasizes the pitfalls of
extrapolating from one species to another, even between close taxonomic relatives.
INFECTIOUS A N D PARASITIC DISEASES
I N T H E VARIOUS FAMILIES O F C A R N I V O R A
CANIDAE
Viral pathogens
Rabies is caused by a rhabdovirus of the genus Lyssavirus, and carnivores serve as
major hosts for this important zoonotic disease. Significant wild canid reservoirs of
rabies include the following:
- red foxes (Vulpes vulpes)
Central Europe (140)
in parts of North America, Asia, and Eastern and
- grey foxes (Urocyon cinereoargenteus)
in parts of North America (74)
- Arctic (blue) foxes (Alopex lagopus) in North America and Asia (124)
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- bat-eared foxes (Otocyon
megalotis)
in South Africa (12, 131)
- coyotes (Canis latrans) in parts of North America (74)
- jackals (C. aureus, C. adustus
140).
and C. mesomelas)
in Africa and Asia (12, 13,
Rabies is transmitted by bite, or by the contact of broken skin with virus-containing
saliva from an affected animal. Diagnosis of rabies in live canids is not possible on
a routine basis, thus the screening of newly-acquired canids is not possible. Recentlycaptured wild canids could be incubating rabies; knowledge of the epizootiology of
rabies in the area of origin is helpful in assessing the risk of introducing rabies to
captive wild animal populations or human caretakers. Rabies is extremely rare in
canids bred in captivity; a minimum quarantine period of 180 days is recommended
for any wild-caught canid (94). Rabies could be introduced into captive canids via
contact with free-ranging or feral species under some types of extrinsic management.
Vaccination of captive wild canids against rabies, using inactivated vaccines, is
appropriate for valuable animals and animals which might be exposed to the virus
(94). Vaccination of humans against rabies is good policy if they will be handling or
caring for wild-caught carnivores.
Canine distemper is probably the most important infectious disease of canids. It has
caused significant mortality in captive canids in zoos (23, 89) and in the fur industry
(23), as well as in free-ranging canids (2, 38). Canine distemper is caused by a
Morbillivirus. The virus is relatively labile in the environment, and is readily
inactivated by solvents, disinfectants, heat and ultraviolet light; half-lives of 1-3 h at
37°C, 2 h at 21°C, and 9-11 days at 4°C have been reported (4). All species of canids
appear to be susceptible to infection, with varying morbidity and mortality; detailed
knowledge of canine distemper in wild canids is lacking. The virus infects a wide
variety of organs and is shed in most excretions of infected animals; transmission
occurs via close direct contact or aerosol. Fomite transmission is possible, but is
unlikely due to the fragility of the virus. Studies in domestic dogs have shown that
incubation varies from 1-3 weeks, with virus being shed as early as 4-5 days
post-infection, possibly continuing for months until either death or complete recovery
occurs (4). The fatality rate for wild canids is not known, but serological surveys
indicate that many canids survive infection (3, 3 1 , 136, 143). Most quarantine
protocols of > 30 days will protect captive populations from introduction of the disease
via canids, but recovered canids which appear clinically normal could shed the virus
and expose susceptible hosts. Captive canids could also contract canine distemper via
exposure to feral domestic dogs or other free-ranging species. Examination of faeces
by negative-stain electron microscopy may detect virus shed in faeces (99), and
serology will give an indication of exposure of captured wild canids. Attenuated
canine distemper vaccines are available for domestic dogs and many have been used
safely in wild canids (15, 127). Some species, however, are exquisitely susceptible to
vaccine-induced disease, including grey foxes (61) and African hunting dogs (Lycaon
pictus) (127). In addition, attenuated vaccines may induce immunosuppression,
leading to secondary infection by opportunistic pathogens. Some attenuated vaccine
viruses may be shed by vaccinated individuals, which could thus potentially transmit
the virus to more susceptible species (89).
Canine parvoviral enteritis is caused by canine parvovirus type 2 (43). This virus
is very hardy in the environment, remains infectious for three months at 20°C, and
may survive in faeces for several years (7). A dilute solution of sodium hypochlorite
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is adequate for sanitation (123). Most species of Canidae appear to be susceptible to
infection, but fatality rates are not known; clinical disease and/or mortality have been
observed in coyotes (44; E.S. Williams, unpublished findings), bush dogs (Speothos
venaticus) (78), crab-eating foxes (Cerdocyon thous) (78), maned wolves (Chrysocyon
brachyurus) (45, 78), raccoon dogs (Nyctereutes procyonoides) (97) and grey wolves
(82, 83, 84). Red foxes and ranched blue foxes are susceptible to infection but appear
to be resistant to disease (9, 97). Juveniles appear to be more susceptible to parvoviral
infection than adults (78, 83). The incubation period in domestic dogs, and probably
wild canids, is 4-7 days (7). Transmission occurs via direct contact with infected
animals and their faeces, which contain abundant virus. Exposure of captive wild
canids might occur via contact with infected domestic dogs, fomites, or other affected
individuals within the captive facility. Periodic shedding may occur in subclinicallyaffected adult animals (66). Quarantine procedures of > 30 days, along with more
specialized tests, are probably adequate to prevent introduction of this disease into
captive facilities from wild-caught or transferred captive canids. Testing faeces for the
presence of virus is possible using antigen capture enzyme-linked immunosorbent
assay (ELISA) techniques or negative-stain electron microscopy. Attenuated
parvovirus vaccines have been used in coyotes (58), maned wolves and bush dogs
(88). Although inactivated vaccines require multiple boosters (66), they may be
preferred (15) if attenuated vaccines have not been shown to be safe in a particular
species.
Infectious canine hepatitis, caused by canine adenovirus type 1, induces infection
and/or disease in foxes (59, 114), coyotes (79) and grey wolves (31). This disease is
probably of little consequence in the wild, but significant mortality has occurred in
ranched foxes. Transmission occurs via direct contact or by ingestion of viruscontaminated material. The virus is shed in urine, faeces and saliva, and by aerosol.
Shedding may be prolonged in domestic dogs (111) and this is likely to be the case
also in wild canids. The incubation period is usually a week or less (57). Attenuated
vaccines are available for domestic dogs; these have been used in captive foxes (57)
and are recommended for wild canids (15). Killed vaccines should be used, unless
attenuated vaccines have been shown to be safe in the species to be vaccinated.
Bacterial pathogens
Brucella spp. infections - probably via consumption of infected prey - have been
reported in wolves, coyotes, foxes, African wild dogs and jackals (39, 4 1 , 150). The
disease is probably subclinical in most carnivores, but birth of weak or stillborn pups
has been observed in wolves (95) and congenital infections may occur in coyotes (39).
Knowledge of the status of wild carnivore prey with regard to brucellosis should help
to determine the testing required for captured wild canids. Transmission between
infected canids and other species is theoretically possible but unlikely. Canids in
captivity for a prolonged period are extremely unlikely to be exposed to Brucella spp.
or to carry the organism.
Wild canids are susceptible to bovine tuberculosis, caused by Mycobacterium
bovis,
but the disease is rare in these species in the wild, unless it is common in their prey.
It is likely that under situations of increased density, stresses related to captivity,
contact with carrier animals, and potential exposure to contaminated feedstuff, canids
could become infected; but they are considered relatively resistant to infection (134).
There are few reports of bovine tuberculosis in captive and free-ranging canids (130;
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J. Rhyan, personal communication). The most likely source of M. bovis infection for
canids in captivity is through contaminated feed. This is unlikely if commercial,
appropriately-processed feed products are used.
Parasites
Wild canids are afflicted by numerous endo- and ectoparasites. Most of these are of
little consequence; some may serve as vectors for zoonotic diseases, however, or cause
clinical disease in young or immunocompromised individuals. Treatment for endo- and
ectoparasites is usually accomplished easily with topical, oral or injectable products
and is recommended when moving canids from the wild to captivity and between
captive facilities, or routinely with captive animals if a parasitic problem is identified.
Sarcoptic mange, caused by Sarcoptes scabiei, is an important disease of wolves,
foxes and coyotes (91, 109, 119, 135, 137). There is a degree of host specificity of the
mites, but experiments have successfully cross-transmitted scabies between wild
canids (119, 128). Humans are also susceptible to infection by S. scabiei from wild
canids (119, 129). Treatment with acaricides is successful (128).
Wild canids may serve as hosts for Trichinella spp., and infestation has been
reported in grey wolves and red foxes from Alaska (115), and in wild carnivores from
north-western North America (60). The normal mode of transmission, via
contaminated feed, is unlikely to occur in captivity as long as uncontaminated or
appropriately-treated diets are fed to carnivores. Capture of infected wild canids is
possible, but under captive conditions they are likely to be dead-end hosts.
The canine heartworm (Dirofilaria immitis) is found in wild canids in areas where
this parasite is present in domestic dogs. D. immitis has been expanding its range and
is endemic in many parts of North America (139). Coyotes (36, 55), red foxes (53, 73,
122), grey foxes (85) and wolves (113) have been reported as hosts. Heartworms are
transmitted via the bite of infected mosquitoes. Prophylactic anthelmintics are
administered to susceptible canids in areas where the parasite is endemic, during
seasons when mosquitoes are present; vector control may also be useful for sensitive
species. Capture of infected wild canids is possible, and - in areas where heartworm
is endemic - captive canids could become infected.
Wild canids are important as definitive hosts of Echinococcus
granulosis and
E. multilocularis (1). The normal sylvatic cycle of E. granulosis involves coyotes and
wolves, and their primary prey - i.e. deer (Odocoileus spp.), moose (Alces alces) and
caribou (Rangifer tarandus). The cycle of E. multilocularis occurs most frequently in
Arctic and red foxes, with microtine rodents as the primary intermediate hosts. These
cestodes form hydatid cysts in intermediate hosts, or in abnormal hosts (e.g. humans).
Infections in humans can be fatal, and therefore treatment of susceptible definitive
hosts from areas with endemic echinococcosis should be part of captive management
plans. Contact of humans and intermediate hosts with faeces from untreated foxes or
other canids should be prevented.
FELIDAE
Viral pathogens
Rabies occurs in wild felids, although these species are not primary reservoirs of the
virus. The above discussion of rabies in wild canids is generally applicable to felids.
Incubation periods of more than two years have been experimentally produced in
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domestic cats (93), although it is not known whether chronic rabies may occur in
non-domestic felids. A quarantine period of six months is required for movement of
domestic cats to the United Kingdom (which is free of rabies) and is recommended
for wild-caught felids (94).
Feline panleukopenia, also called feline distemper or feline infectious enteritis, is
caused by a parvovirus. The disease agent is closely related to canine parvovirus, mink
enteritis virus and raccoon enteritis virus (104). Probably all Felidae are susceptible
to feline panleukopenia (14) and the disease has occurred in many captive species
under a variety of management conditions (88). Cats which recover from
panleukopenia may shed the virus in faeces for weeks, and the virus may persist at low
levels for more than a year (35). Quarantine periods of > 30 days are probably
adequate for cats. The most frequent source of feline panleukopenia virus for captive
felids is probably direct or indirect contact with domestic cats (88). The virus is very
resistant to environmental conditions and may remain infective for months or years.
All captive cats should be vaccinated to prevent feline panleukopenia (15). Inactivated
vaccines should probably be used (28), unless attenuated vaccines have been shown
to be safe in the species of interest; some non-domestic cats, including the bobcat
(Felis rufus) (E.S. Williams, unpublished findings), may be susceptible to attenuated
vaccines, while studies with cheetahs (Acinonyx jubatus) demonstrated the safety of
an attenuated virus vaccine (126, 138).
Feline leukaemia virus, a retrovirus of felines, is common in domestic cats; but little
is known about the disease in non-domesticated wild felids, except that some are
susceptible to infection (19, 20, 67, 134). In domestic cats, the virus causes a variety
of syndromes ranging from
neoplasia
to reproductive
problems
and
immunosuppression (106, 134). Transmission occurs via direct contact with carriers;
in utero transmission may occur in domestic cats. Oral transmission via prEdation of
domestic cats has been suspected in a mountain lion (Felis concolor) (67). Measures
should be taken to prevent introduction of this virus into collections of non-domestic
felids, due to the significant disease problems associated with this virus in domestic
cats and the lack of treatment or of proven efficacy of vaccination in non-domestic
felids. Serological screening of wild cats is recommended. Routine vaccination of
non-domestic felids is not recommended, although vaccination might be justified in
specific circumstances (20).
Feline immunodeficiency virus is a newly-recognized retrovirus (107) which infects
a variety of wild felids as well as domestic cats. Relatively little is known about the
relationship between this virus and wild hosts, although some populations of wild
felids show high seroprevalence (21, 22, 76, 102). In domestic cats, feline
immunodeficiency virus may cause subclinical infection or immunosuppression, with
resultant increased susceptibility to other pathogens and opportunistic infections.
Serological surveys have demonstrated that the virus is common in some free-ranging
populations of mountain lion, lion (Panthera leo), leopard (P. pardus) and cheetah, but
appears to be less common in captive populations (11, 21). The implications of the
presence of this virus in wild cats are not yet known; as feline retroviruses are
essentially carried for life, however, and could be transmitted horizontally, serological
testing and exclusion of seropositive animals may be justified.
The causative agent of feline infectious peritonitis (a feline Coronavirus), or
antibodies against this virus, have been reported in many wild felids (153). Much
attention has focused on cheetahs, in view of the marked susceptibility of this species
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to feline infectious peritonitis virus (22, 63), which is perhaps due to limited genetic
variability (92, 100). Vaccines have not been approved for use in non-domestic cats.
Some captive non-domestic cat facilities require serum antibody tests and electron
microscopy of faecal samples prior to introduction of new animals (153).
Canine distemper is discussed in greater detail above (see 'Canidae'). This virus has
recently been recognized as a significant pathogen of captive lions, tigers (Panthera
tigris) and leopards (8, 152), and free-ranging lions (90). Susceptibility of domestic
cats to experimental canine distemper has been recognized (5), but this was considered
unusual. A few deaths in captive wild felids were reported as early as 1983, in a Bengal
tiger (P. tigris tigris) (16) and a Siberian tiger (P. tigris altaica) (54). Possible sources
of canine distemper virus include contact with free-ranging and feral canids, raccoons
(Procyon lotor) (8), or any of numerous other susceptible free-ranging species. At
present, little is known about the susceptibility, transmission and pathogenesis of
canine distemper in wild felids. Vaccination with inactivated canine distemper
vaccines may be considered if exposure is possible; attenuated vaccines have not yet
been tested for safety and efficacy in wild felids.
Several respiratory viral diseases occur in captive wild cats, including feline viral
rhinotracheitis caused by feline herpesvirus type 1 and feline calicivirus infection (47).
Feline herpesvirus has been isolated from cheetah (121, 132) and clouded leopard
(Neofelis nebulosa) (18). Transmission of these viruses usually occurs via direct
contact and possibly via fomites; high densities of cats in a captive situation probably
increase transmission. Cats which have recovered from feline herpesvirus infections
could infect other cats. Vaccines developed for domestic cats have been tested and
used successfully in non-domestic cats (28, 126, 138).
Pseudorabies (Aujeszky's disease), caused by a herpesvirus, is a minor
consideration in captive non-domestic cats. This disease has most frequently been a
problem in Central and Eastern Europe (56). In species other than swine, Pseudorabies
is manifest as 'mad itch'. Swine are the major reservoir, and wild felids may develop
Pseudorabies following direct or indirect contact with swine, particularly by ingestion
of pork (50, 56). The virus may survive in muscles of carcasses for 11-36 days (56)
but the disease can be effectively prevented in wild felids by providing appropriatelyprocessed diets.
Feline spongiform encephalopathy is a recently-identified member of the
spongiform encephalopathy group of infectious diseases. Cases in captive cheetah
(108) and mountain lion (148) have been associated with the bovine spongiform
encephalopathy epizootic in Great Britain. Epidemiological evidence suggests that the
cats were exposed via contaminated feed in Great Britain, and there is no evidence to
date of horizontal or vertical transmission among non-domestic cats. The occurrence
of a case in a cheetah imported to Australia (108) highlights the potential for moving
unrecognized disease inadvertently over long distances.
Bacterial pathogens
Plague, caused by Yersinia pestis, may infect and cause illness and mortality in
felids. Wild and domestic cats serve as a link between wild rodent plague and humans
in North America (10). Unlike most carnivores, cats appear to be relatively susceptible
to clinical disease induced by Y pestis. Approximately 3 8 % of experimentally-infected
domestic cats succumbed to plague; the bacteria could be cultured from the oral cavity
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for ten days post-inoculation (49). An adequate quarantine period for wild felids
captured from areas with sylvatic plague - based on findings from experimental
infections of domestic cats - is two weeks. It is recommended that wild felids from
plague endemic areas be treated for fleas, as these could potentially harbour Y. pestis.
Bovine tuberculosis may occur in captive wild felids; cats are considered to be more
susceptible to M. bovis infection than canids (134). Wild felids most likely contract
tuberculosis from contaminated meat and offal. Unfortunately, diagnostic tests are not
considered accurate in wild felids, and usual quarantine periods may not prevent the
introduction of M. bovis into captive populations. Establishing the origin of wild felids
and the possibility of exposure to tuberculosis before introduction into captive
populations is prudent.
Anthrax, caused by Bacillus anthracis, has caused mortality in captive wild felines
(46), particularly cheetahs (65). The route of transmission to these captive cats was via
contaminated food. Use of appropriately-prepared foodstuffs should prevent the
introduction of anthrax to captive felids.
Parasites
Endo- and ectoparasites in captive wild felids are relatively easy to treat topically,
orally or by injectable preparations (118).
Wild felids can act as hosts for Trichinella spiralis (40, 154); due to the oral route
of transmission, however, incorporation of an infected animal into captivity is unlikely
to result in establishment of the parasite in captive populations. The potential
introduction of Trichinella spp. into captive felids via contaminated foodstuffs,
however, is a greater problem. Appropriate treatment of feed will reduce the chances
of introducing this parasite into captive animals.
Most cestode parasites of wild felids are innocuous, with a few exceptions. Canids
and rodents are the usual hosts of Echinococcus multilocularis (34), but wild felines
may occasionally be infected (75). The parasite does not cause significant disease in
cats. Humans, however, could be infected by contact with cat faeces which contain
eggs (34), and untreated infections may be fatal in humans (149). Anthelmintic
treatment is appropriate for animals removed from the wild; reinfection is unlikely to
occur in captivity, unless the cats have access to infected intermediate rodent hosts.
Many wild and domestic cats are infected with Toxoplasma gondii (118), although
toxoplasmosis is rare in cats. Transmission occurs via ingestion of infective oocysts
or consumption of secondary hosts (e.g. mice and rats) harbouring protozoal cysts.
Infected cats may be identified by faecal examination for oocysts. Oocysts are
relatively resistant to environmental conditions and could be transmitted to in-contact
species, some of which may be highly susceptible to toxoplasmosis, e.g. Callitrichidae
(151) or black-footed ferrets (26).
MUSTELIDAE
Viral pathogens
Skunks (Mephitis mephitis) are one of the primary reservoirs of rabies in North
America (74), but all species of mustelids are considered susceptible. The observations
about rabies in Canidae and Felidae also apply to Mustelidae. A rabies vaccine has
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recently been approved for use in domestic ferrets (Mustela putorius furo) in the
United States of America (USA) (94). Inactivated vaccines are also appropriate for use
in valuable non-domestic mustelids or in those which could be exposed to the virus
by virtue of their housing.
Canine distemper is the most important viral infection of mustelids, although the
fatality rate in each species is not known. Some, such as the black-footed ferret, are
exquisitely susceptible to fatal infection (143). Based on the presence of seropositive
individuals, other species appear to be somewhat resistant and to survive infection.
Features of canine distemper in mustelids are similar to those in canids (23).
Attenuated canine distemper vaccines prepared in avian cell lines have been used
successfully in American badgers (Taxidea taxus) (51) and other mustelids (15).
However, attenuated vaccines are not safe in all species (29). In addition to the risk
of vaccine-induced canine distemper, attenuated vaccines induce immunosuppression
in mustelids (69, 77). Quarantine periods of > 30 days are probably adequate to
prevent introduction of canine distemper via wild-caught mustelids. Free-ranging
black-footed ferrets and American badgers have been found to be incubating canine
distemper when captured (143; D. Hoff and E.S. Williams, unpublished findings).
Parvoviruses cause several significant diseases in mustelids. Mink enteritis virus is
closely related to feline panleukopenia virus and has caused significant disease in
ranch mink (Mustela vison) (25). Mink are also susceptible to feline panleukopenia
virus, but skunks are resistant to both feline panleukopenia virus and mink enteritis
virus (9). Vaccines are available for mink virus enteritis and are commonly used on
fur farms.
Aleutian disease, also caused by a parvovirus, is an important disease in farmed
mink, particularly animals of the Aleutian colour phase (105). Skunks (64), domestic
ferrets (71, 72, 101, 112, 141), and possibly otter (Lutra lutra) (142) and other species
(72) are also susceptible to strains of this virus. Transmission occurs via direct contact,
fomites or vertical transmission. Transmission is suspected to have occurred via
inadequately-cleaned cages after several years (37). The virus is shed in saliva, urine
and faeces (52) for long periods; but it is not considered highly contagious (105),
although high densities of animals increase transmission. As with all parvoviruses,
Aleutian disease virus is very resistant to environmental inactivation (105). In the fur
industry, where Aleutian disease has caused the greatest problems, test and slaughter
programmes have been used to eradicate the disease on premises, and testing followed
by isolation or removal has been suggested for commercial ferret facilities (103). This
may not be possible in groups of valuable or endangered captive mustelids; in such
circumstances, serological testing of animals and exclusion from the facility of those
which are seropositive should be used to prevent introduction of the disease. As
Aleutian disease is more severe in the Aleutian genotype than in standard mink, it is
possible that endangered, possibly inbred, mustelids could be seriously affected by this
virus.
Transmissible mink encephalopathy is a member of the spongiform encephalopathy
group of diseases (81). This disease is rare in the mink industry, but it is of interest
in view of the similarity to bovine spongiform encephalopathy, scrapie and human
diseases. Transmissible mink encephalopathy is transmitted orally via consumption of
contaminated feed - possibly contaminated with the agent of scrapie - (62, 80) or via
cannibalism (24). The disease has been experimentally reproduced in other mustelids
(81). There is no evidence of natural transmission by means other than contaminated
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feed, and use of uninfected feed for mustelids should therefore prevent introduction
of the disease to captive animals. While spongiform encephalopathy in wild felids
occurred during the recent bovine spongiform encephalopathy epizootic in Great
Britain, there was no report of spongiform encephalopathy in mustelids.
Bacterial pathogens
Mustelids are susceptible to bovine tuberculosis, and may serve as significant wild
reservoirs of the disease. Tuberculosis has been reported in free-ranging European
badgers (Meles meles) (32) and feral domestic ferrets in Great Britain and New
Zealand, respectively. These species could become infected in captivity via contact
with tuberculous individuals or contaminated feed.
URSIDAE
There are few reports of infectious diseases in captive Ursidae, suggesting either
that bears are unusually resistant to the variety of pathogens which affect the other
carnivore families or, more probably, that they have not been studied in such great
detail.
Viral pathogens
Bears appear to be relatively susceptible to infection, and mortality due to infection
with Pseudorabies virus has occurred in brown bears (Ursus arctos) (V. Guberti,
personal communication). Pseudorabies in bears is similar to that in other carnivores
(see 'Felidae' above). Avoiding contaminated feed - particularly fresh swine products
in areas where Pseudorabies is endemic — should prevent introduction of the disease
to captive bears.
Canine adenovirus type 1, or canine hepatitis virus, has caused mortality in captive
black bears (U. americana) (114). Bears may be susceptible to attenuated vaccines
(46). Canine adenovirus may cause significant illness and death, or may lead to
subclinical infection. The source of the virus in captive bears is most likely to be
contact with infective feral or captive canids.
Parasitic pathogens
Infection by T. spiralis is found in wild (154) and captive bears (118). Fowler (46)
reported an infected polar bear (U. maritimus) after at least ten years of captivity. In
captivity, these animals are dead-end hosts. Trichinella-infected rodents could be
sources of infection for captive carnivores (118).
PROCYONIDAE
Viral pathogens
Raccoons are important reservoirs of rabies in eastern North America (74). The
recent outbreak in the north-eastern U S A serves as a dramatic example of the dangers
of movement of wild animals without appropriate regulation and quarantine; rabid
101
raccoons were inadvertently introduced into West Virginia from the south-eastern
USA. Free-ranging raccoons could be a source of rabies for captive wild species in
endemic areas.
Canine distemper is the most important viral infection of procyonids in captivity and
the wild (23). All species appear to be susceptible to infection, and some appear to be
particularly susceptible; vaccine-induced canine distemper has been reported in
kinkajous (Potos flavus) (70) and red pandas (Ailurus fulgens) (27). Attenuated canine
distemper vaccines may be immunosuppressive in procyonids; a red panda died due
to an opportunistic infection following vaccination (87). Sources of canine distemper
in captive procyonids are contact with infected feral or other captive species. Degree
of risk is dependent on the management of the animals.
Raccoons are susceptible to feline panleukopenia virus and mink enteritis virus (9),
and a closely-related raccoon parvovirus (96), but do not develop clinical signs
following infection with canine parvovirus (6, 9). Other procyonids (88) are probably
susceptible to parvoviral enteritis, although this is seldom reported in the literature.
Experimental and natural Pseudorabies infections have been reported in raccoons
(110). Transmission of the virus between raccoons by direct contact (110) suggests that
this species could serve as a reservoir, but most raccoons are probably dead-end hosts.
Captive procyonids could contract the disease via contact with infected swine.
Parasitic pathogens
Internal parasites are common in procyonids, and include some (e.g. Baylisascaris
procyonis) (120) which may be pathogenic in other animal species and in humans.
Anthelmintic treatment of captive procyonids should be routine in areas where
parasites are a problem.
VIVERRIDAE A N D HYAENIDAE
Viral pathogens
Very little information is present in the literature on diseases of viverrids and
hyenas. Reviews suggest that species in these families are susceptible to the same
diseases as canids and felids (42, 116). These comments highlight how little is known
about diseases of these animals.
Mongooses (Cynictis penicillata, Herpestes auropunctatus) are important reservoirs
of rabies in Africa and the Caribbean (30, 74). Rabies also has been reported in hyenas
(Crocuta crocuta) in Africa (86). Concerns about the capture of wild viverrids and
hyenas which are incubating rabies are similar to those observed for the other
carnivore families, and lengthy quarantine periods may be appropriate (94). Species
in these families are assumed to be susceptible to canine distemper (23) and
parvoviruses (88), but this is based on few reports. As with other species, use of
inactivated vaccines is recommended unless attenuated vaccines have been shown to
be safe in a particular species. Those studying or managing viverrids and hyenas
should be encouraged to publish information on disease susceptibility in these species.
102
D I S E A S E IN B L A C K - F O O T E D F E R R E T S
The history of the endangered black-footed ferret in captivity provides a good
illustration of the real and potential problems with infectious and parasitic diseases
which face managers of captive wild species, and of the interface between the wild and
captivity. This also demonstrates the usefulness, but also the problems, of assuming
that diseases of closely-related species - e.g. domestic ferrets or Siberian polecats
(M. eversmanni) - will be the same as those of black-footed ferrets. Captive blackfooted ferrets are susceptible to a number of diseases, and management practices
therefore attempt to minimize the introduction of exotic pathogens into the captive
population and hence into the wild via reintroduction. Understanding of the disease
susceptibility of black-footed ferrets continues to increase over time.
Recovery efforts for the black-footed ferret have involved removal to captivity of
members of this species from the last known wild population, in Wyoming (USA),
followed by an aggressive captive breeding programme and return of animals to the
wild. Management of infectious diseases has played an important and varying role in
all phases (145).
Viral pathogens
The real threat of moving infectious diseases from the wild to captivity along with
free-ranging individuals was exemplified by the experience with six black-footed
ferrets captured in 1985 for captive breeding. Two wild-caught black-footed ferrets
were incubating canine distemper; these animals subsequently died, as did four
in-contact animals (133, 143). Canine distemper is the most important infectious
disease of mustelids, especially in highly-susceptible black-footed ferrets. Although
impractical in some situations, individual (rather than group) isolation for quarantine
could prevent transmission of canine distemper between recently-captured animals.
Extensive disease prevention precautions are in place through the Black-Footed Ferret
Species Survival Plan, which requires that the animals be kept in isolation facilities,
and that personnel must take a shower or change clothing, as well as wearing a
face-mask and disinfecting their hands, prior to contact with black-footed ferrets (145).
This is necessitated by several factors, namely the ubiquitousness of canine distemper
virus, the relatively small population of black-footed ferrets, the 100% mortality
expected from this disease in susceptible animals, and the absence of a completely
effective vaccine. Inactivated canine distemper vaccines are used in black-footed
ferrets (145), but in trials with black-footed ferret x Siberian polecat hybrids,
morbidity and mortality occurred following challenge with virulent virus (77, 147).
Some attenuated vaccines induce canine distemper in black-footed ferrets (29;
E.S. Williams, unpublished findings) and may induce significant immunosuppression
(77). Research is continuing for the development of a safe and effective vaccine.
Rabies is always a consideration when moving carnivores from the wild to captivity.
In the case of the black-footed ferret, rabies was not considered to be a significant
threat. The distribution of rabies in wild and domestic animals is well known in
Wyoming, due to continuous diagnostic surveillance for this disease. The source
population of captive black-footed ferrets was from an area where no cases of rabies
had been reported. This exemplifies the usefulness of background information on the
occurrence and distribution of animal diseases when collecting free-ranging animals
for captivity.
103
Aleutian disease virus is considered a potential pathogen of black-footed ferrets and
one which could have serious ramifications on wild and captive populations. The
disease is currently absent in the captive population, and Species Survival Plan
management of the animals seeks to prevent its introduction. Black-footed ferrets are
isolated from other mustelids (particularly mink or other ferrets) not shown to be free
of Aleutian disease. Siberian polecats - maintained for cross-fostering purposes,
breeding experience (for the males) and research - were from an Aleutian disease-free
population. Contact between black-footed ferrets in outside facilities and free-ranging
mustelids is prevented by the use of double fencing. Serological screening for Aleutian
disease antibodies is recommended in the future, if animals are moved from the wild
to captivity, or within the captive population if the Species Survival Plan disease
prevention protocol is changed. This is particularly true as at least one of the
black-footed ferret reintroduction sites contains seropositive skunks (E.S. Williams,
unpublished findings).
Human influenza has been documented as causing disease in domestic ferrets (48).
Thus, when caretakers of black-footed ferrets are ill they do not handle the animals,
and all handlers wear face-masks and disinfect their hands when in direct contact with
these animals. To date, influenza has not been observed in black-footed ferrets.
Introduction of enteric diseases is of concern, due to the susceptibility of domestic
ferret kits to rotavirus-induced morbidity and mortality (48). Rotavirus has been
suspected in some cases of diarrhoea in black-footed ferrets, where virus has been
demonstrated by negative-stain electron microscopy and by antigen capture ELISA
(E.S. Williams, unpublished findings). It is possible that rotavirus carriers were
brought in from the wild, that rotaviruses were introduced via food contaminated with
the virus, or that the virus was introduced via fomites. Isolation procedures, including
the use of footbaths and showers, serve to decrease the possibility that enteric viruses
will be introduced.
The apparent heightened susceptibility of black-footed ferrets to a number of
infectious disease agents has raised concerns about retroviral infections. Some of these
viruses are known to cause significant immunosuppression in other species. The
authors are currently testing black-footed ferret sera and tissues for evidence of
retroviruses. These viruses could cause significant damage to captive propagation
efforts for this endangered species. Introduction of retroviruses should therefore be
prevented by isolation and lack of contact with other mustelids.
Bacterial pathogens
The most serious bacterial disease of black-footed ferrets is plague (146). The
recently-recognized susceptibility of black-footed ferrets to plague exemplified the
need to be cautious in extrapolating the significance of disease in closely-related
species (e.g. domestic ferrets) which are resistant to parenteral challenge with Y. pestis
(144). Risk of this disease is minimized in the captive environment by strict quarantine
procedures for prairie dogs (Cynomys spp.), which form part of the diet of black-footed
ferrets (145), and by the use of isolation facilities. Wild-caught prairie dogs are
maintained in quarantine for at least ten days, which is considered to be longer than
the incubation period of plague in white-tailed prairie dogs (E.S. Williams,
unpublished findings), and necropsy is performed on all animals which die during
quarantine to determine the cause of death. This not only serves to ensure that the
104
black-footed ferrets have a food source which is free of plague, but also reduces the
danger to the humans who handle and process the prairie dogs and care for the captive
black-footed ferrets.
Black-footed ferrets in external cages in locations with endemic plague are not
protected from this disease (146). While these cages prevent the escape of black-footed
ferrets and the entry of large species, small free-ranging rodents - some of which
might carry plague - could gain access to the cages. Black-footed ferrets which have
been in external cages are not returned to the breeding colony until they have
completed a six-week quarantine period in individual isolation.
Parasites
Parasites of black-footed ferrets and their prairie dog prey have been studied (17,
68, 117, 125). Internal parasites probably constitute the greatest disease management
problem in black-footed ferrets on a day-to-day basis. Eimeria ictidea and E. furonis
are natural parasites of black-footed ferrets (68), and coccidiosis is a problem primarily
in young ferrets (kits) (145). The latter problem is managed by attention to sanitation
and by treatment with anticoccidial agents when clinical signs are apparent. Even with
good sanitation, the method of management of these animals - with nest boxes and
artificial tunnels to simulate prairie dog burrows - does not totally prevent contact of
kits with faeces and hence with the parasite.
Another important parasite of captive black-footed ferret kits and a few adults is
Cryptosporidium sp., which causes ill thrift and mucoid diarrhoea. This parasite was
not anticipated to be a significant pathogen of black-footed ferrets, on the basis of
information on known diseases of mustelids. It is not known whether the parasite is
natural in this species (i.e. present in free-ranging populations prior to their capture),
or whether black-footed ferrets acquired this parasite in captivity. Cryptosporidium is
a very common parasite and could have been introduced through food, contact with
human carriers, or water. There are no specific treatments for this parasite, although
some antibiotics - azithromycin, in particular - have shown some efficacy in reducing
clinical disease in captive black-footed ferrets (E.S. Williams et al., unpublished
findings).
An outbreak of toxoplasmosis was documented at one captive breeding facility (26).
Source of infection was not definitively determined but was felt to be associated with
rabbit meat used in the diet. This outbreak appeared to be due to a single exposure to
the pathogen; the disease has not recurred in this or other captive breeding facilities.
In addition, there has been no clinical evidence of transmission from black-footed
ferret dams to offspring. This outbreak served to highlight several points about disease
and captive maintenance of endangered species: first, some of these species may have
a heightened degree of susceptibility by virtue of the degree of inbreeding, the stresses
of captivity, or infection by immunosuppressive agents; and second, that - even with
relatively strict quarantine procedures — introduction of significant pathogens is
possible and surveillance should therefore remain high.
*
*
*
105
LES MALADIES INFECTIEUSES ET PARASITAIRES DES CARNIVORES VIVANT
EN CAPTIVITÉ, ET PARTICULIÈREMENT DU PUTOIS D'AMÉRIQUE
(MUSTELA NIGRIPES). - E.S. Williams et E.T. Thorne.
Résumé : Les carnivores vivant en captivité peuvent souffrir d'une grande
variété de maladies infectieuses et parasitaires, en raison de la diversité des
sept familles de Carnivores. Malheureusement, rares sont les études
approfondies portant sur les maladies des espèces non domestiques de
carnivores, et beaucoup de lacunes subsistent, notamment en ce qui concerne
les maladies affectant les petits carnivores (c'est-à-dire les mustélidés, les
viverridés et les procyonidés). Les principales maladies des carnivores sont la
rage, la maladie de Carré et les infections dues à des parvovirus, des
Coronavirus et des herpesvirus. Les maladies parasitaires ou bactériennes ne
présentent guère de danger pour les populations élevées en captivité, et un
élevage correctement mené, l'application de médicaments, la vaccination et la
quarantaine suffisent à réduire le risque de maladie. S'agissant de la
susceptibilité à l'égard des agents pathogènes, la connaissance que l'on a
d'une espèce peut induire en erreur lorsqu'on l'applique à une autre espèce. Le
putois d'Amérique (Mustela nigripes) est un exemple de carnivore
particulièrement touché par des maladies infectieuses, dont certaines sont
prévisibles tandis que d'autres ne peuvent l'être à partir de la seule
connaissance des maladies des autres mustélidés. Ceci souligne le besoin de
mieux comprendre l'histoire naturelle de chaque espèce maintenue en captivité.
MOTS-CLÉS : Canidés - Carnivores - Félidés - Hyénidés - Maladies
infectieuses - Mustela nigripes - Mustélidés - Procyonidés — Putois
d'Amérique - Ursidés - Viverridés.
*
*
*
ENFERMEDADES INFECCIOSAS Y PARASITARIAS DE CARNÍVOROS EN
CAUTIVIDAD, CON ESPECIAL REFERENCIA AL TURÓN PATINEGRO
(MUSTELA NIGRIPES). - E.S. Williams y E.T. Thorne.
Resumen: Los carnívoros en cautividad son sensibles a un amplio espectro de
enfermedades infecciosas y parasitarias, hecho que refleja la diversidad
existente entre las siete familias del orden Carnivora. Por desgracia, los
estudios sobre las enfermedades de los carnívoros no domésticos son
relativamente escasos y queda mucho por aprender, en especial sobre las
enfermedades de los pequeños carnívoros (por ejemplo los mustélidos,
vivérridos y prociónidos). Entre las enfermedades infecciosas más importantes
de los carnívoros se encuentran la rabia, el moquillo canino y las afecciones
causadas por parvovirus, Coronavirus y herpesvirus. Pocos son los patógenos
bacterianos o parasitarios importantes en lo que concierne a las poblaciones
cautivas, y las adecuadas prácticas de manejo, terapia, vacunación y
cuarentena minimizan el riesgo de enfermedad. Las extrapolaciones de una
especie a otra sobre la sensibilidad a enfermedades pueden resultar
incorrectas. El turón patinegro (Mustela nigripes) constituye un ejemplo de
carnívoro especialmente afectado por enfermedades infecciosas, algunas de las
cuales eran previsibles, mientras que otras no podían preverse a partir del
conocimiento general de las enfermedades que afectan a los mustélidos. Esto
pone de relieve la necesidad de comprender la historia natural de cada una de
las especies mantenidas en cautividad.
106
PALABRAS CLAVE: Canidae - Carnivora - Enfermedades infecciosas Felidae - Hyaenidae - Mustela nigripes - Mustelidae — Procyonidae — Turón
patinegro - Ursidae - Viverridae.
*
* *
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