diseases of wild animals transmissible to domestic animals

Rev. sci. tech. Off. int. Epiz., 1988, 7 (4), 705-736.

Diseases of wild animals transmissible to domestic animals

P.-P. PASTORET, E. THIRY, B. BROCHIER, A. SCHWERS, I. THOMAS and J. DUBUISSON *

Summary: The authors have reviewed reports submitted by 22 Member Countries of the OIE concerning diseases of wild animals transmissible to domestic animals, and have outlined the main trends. It is emphasised that many infections and infestations are specific and are not transmitted from wild to domestic species. Diagnostic and epidemiological tools are often unsuitable, and false conclusions may be drawn from their results. While attention may be focussed on the transmission of certain diseases from wild to domestic animals, the reverse also applies, particularly in view of the considerable improvement in the economic status and cultural appreciation of wild animals in recent years. In some cases, intervention may be necessary to improve the health of wild species, particularly in disturbed ecological systems.

Certain diseases are selected for detailed consideration because of their importance, such as malignant catarrhal fever, African swine fever, foot and mouth disease (in Africa), African horse sickness and pestiviral infections.

The authors conclude that it is necessary to reshape thinking in veterinary circles concerning the approach to disease problems created by wildlife. The role played by wildlife must be reconsidered, and specific research programmes must be initiated to develop more suitable diagnostic, epidemiological and conceptual tools.

KEYWORDS: Animal diseases - Animal resources - Animal welfare - Disease control - Disease transmission - Domestic animals - Ecosystems - Epidemiology -Game ranching - Veterinary research - Wild animals - Zoonoses.

I N T R O D U C T I O N

The problem created by diseases of wild animals transmissible to domestic animals is complicated for many reasons.

Firstly, the infections or infestations which may be exchanged are relatively numerous and of various types, comprising viral, bacterial and parasitic diseases. Some of them are also transmissible to man , which further complicates the problem.

Next, the economic, geographical and ecological situations which permit reciprocal transmission are extremely variable, as is also the degree of intensification of animal

* Département de Virologie-Immunologie, Faculté de Médecine vétérinaire de l'Université de Liège, 45, rue des Vétérinaires, B-1070 Brussels, Belgium.

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production, whether in domestic or wild species. The extent of surveillance and diagnostic activities is also varied.

Finally, whereas a situation may be relatively simple from the aspect of domesticated species, the same may not apply to the wild species, given the differences in their variety and population density.

The problem is complicated further because certain wild species are bred in captivity under ranching or farming conditions. Examples can be cited in industrialised countries (such as deer in Scotland) and in African countries (such as Zimbabwe). Certain wild species may be introduced into a country for subsequent release or maintenance in captivity, and this creates difficulties from the aspect of international t rade. Others may be bred in order to repopulate game reserves. In recent years these aspects have become quite important , and so they will be dealt with separately in this report .

It should be noted that the problem does not flow in one direction only, so that in addition to considering the risks posed by wildlife for domestic animals, it is also necessary to consider domestic species as sources of risk to wildlife. The most striking example of the latter is the spread of rinderpest throughout the African continent at the end of the last century (108, 89), and its often dramatic extension to big game.

Fortunately, examples as spectacular as this are rare, and it is true to say that , although the infections or infestations shared by wildlife and domestic animals and /o r man are numerous , they are still a minority. In fact, most infections (particularly viral diseases and parasitoses) are not shared but are strictly specific, being confined to a single species or to closely related species.

The specificity of infections and infestations has not always been recognised, and even today prophylactic measures sometimes fail to take it into account. This raises a special problem which will be dealt with later in this report . The specificity of infections is well illustrated by the case of Australia, where problems arise not from the indigenous mammals (marsupials) but from introduced placental mammals which have reverted to the feral state. In addition, it is unfortunate that there is often little knowledge of the actual susceptibility of wild species to the pathogens of domestic animals.

This report commences with a review of information provided by twenty-two Member Countries (or territories) of the OIE and placed at our disposal by that organisation. It continues with an account of problems selected because of their importance, and of diseases which play a major role.

It ends with a concise summary of the information, general conclusions and several recommendations. The complexity of the problem is such that it is impossible to provide an exhaustive account within the limited extent of this review. Our presentation is thus confined to an outline of the essential features.

LIST OF T H E P R I N C I P A L D I S E A S E S C O N S I D E R E D

Table I shows the principal diseases mentioned in the various reports, together with the country supplying the information and the wild species which may act as source.

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It is regrettable that few of the reports use the internationally accepted Latin names of species. In some cases it has proved difficult to define the species involved simply from the vernacular name.

The diseases are classified according to List A and List B of the OIE. We have added a third list for information concerning infections not usually contained in the official lists.

T A B L E I

Principal diseases, countries affected and susceptible wild species

Country which Wildlife species Disease name provided and (when applicable)

information susceptibility of man

LIST A DISEASES

Foot and mouth disease

Vesicular stomatitis

Rinderpest

Uganda

South Africa

Zambia Zimbabwe Bulgaria Switzerland USSR

USA

Uganda

South Africa

African buffalo (Syncerus caffer)

African buffalo (Syncerus caffer) Impala (Aepyceros melampus) Greater kudu (Tragelaphus strepsiceros) African buffalo (Syncerus caffer) African buffalo (Syncerus caffer)

Wild boar (Sus scrofa) in 1960 Saiga antelope (Saiga tatarica)

A zoonosis

Feral pigs, wild boar (Sus scrofa) and other species

African buffalo (Syncerus caffer) Warthog (Phacochoerus aethiopicus) Species particularly susceptible: African buffalo (Syncerus caffer) Warthog (Phacochoerus aethiopicus) Eland (Tragelaphus oryx) Greater kudu (Tragelaphus strepsiceros) Very susceptible species: Bushbuck (Tragelaphus scriptus) Bush pig (Potamochoerus porcus) Giraffe (Giraffa camelopardalis) Sitatunga (Tragelaphus spekei) Bongo (Tragelaphus euryceros) Gnu (Connochaetes spp.) Giant forest hog (Hylochoerus meinertzhageni)

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T A B L E I (contd.)

Disease name Country which

provided information

Wildlife species and (when applicable) susceptibility of man

Rinderpest (contd.)

South Africa (contd.)

Lumpy skin disease

Togo

South Africa

Moderately susceptible species: Reedbuck (Redunca spp.) Tsessebe or topi (Damaliscus lunatus) Blesbok (Damaliscus dorcas albifrons) Bontebok (Damaliscus dorcas pygargus) Gemsbok (Oryx gazella) Roan antelope (Hippotragus equinus) Sable antelope (Hippotragus niger) Oribi (Ourebia ourebi) Impala (Aepyceros melampus) Springbok (Antidorcas marsupialis) Species not very susceptible: Common Waterbuck (Kobus ellipsiprymnus) Duikers (Cephalophus spp.) Beisa oryx (Oryx beisa) Grant's gazelle (Gazella granti) Dik-dik (Madoqua spp.) Red hartebeest (Alcelaphus buselaphus) Fairly resistant species: Thomson's gazelle (Gazella thomsoni) Hippopotamus (Hippopotamus amphibius) Gerenuk (Litocranius walleri) African buffalo (Syncerus caffer) Absent in wildlife

Rift Valley fever

South Africa

Bluetongue South Africa

USA

Australia

A zoonosis

African buffalo (Syncerus caffer) Springbok (Antidorcas marsupialis) Blesbok (Damaliscus dorcas albifrons) Monkeys and rodents Serological evidence in: hippopotamus (Hippopotamus amphibius) and the African elephant (Loxodonta africana)

Specific antibodies are present in most African artiodactylids, African elephant (Loxodonta africana) and various rodents White-tailed deer (Odocoileus virginianus) Mule deer (Odocoileus hemionus) Often confused with epizootic haemorrhagic disease of Cervidae Feral cattle and water buffalo


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African horse sickness

African swine fever

Classical swine fever

Fowl plague

Newcastle disease

South Africa

Uganda

South Africa

Zambia

Zimbabwe

Bulgaria

USSR

Australia New Caledonia United Kingdom

USA Australia

New Caledonia France

United Kingdom

Sweden

USSR

Zebra (Hippotigris)

Warthog (Phacochoerus aethiopicus) Bush pig (Potamochoerus porcus) Soft tick (Ornithodoros moubata) Warthog (Phacochoerus aethiopicus) Bush pig (Potamochoerus porcus) Giant forest hog (Hylochoerus meinertzhageni) Warthog (Phacochoerus aethiopicus)

Wild boar (Sus scrofa)

Surveillance of wild birds Surveillance of wild birds Aquatic birds

A zoonosis

Surveillance of birds Surveillance of birds Serological evidence of infection in wild birds Surveillance of birds Semi-domesticated pigeons (Columba livia) Semi-domesticated pigeons (Columba livia) Semi-domesticated pigeons (Columba livia) Wild birds

Anthrax

Aujeszky's disease

LIST B DISEASES

A zoonosis

South Africa

USA

Disease particularly spread by flies; rare species in game parks, such as the roan antelope (Hippotragus equinus), are vaccinated

Feral pigs

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Aujeszky's disease (contd.)

Echinococcosis-hydatidosis

Heartwater

Leptospirosis

Mexico USSR

Australia

Bulgaria Portugal

Switzerland USSR

South Africa

Zimbabwe


A zoonosis

Typical cycle between domestic dogs and sheep, also a wildlife cycle in dingoes, stray dogs and the kangaroo family (Macropodidae)

Fox (Vulpes vulpes) Wolf (Canis lupus) Wild boar (Sus scrofa)

Carnivores

Tick-transmitted; tortoises may serve as a sylvatic reservoir by harbouring early stages of the vector, Amblyomma hebraeum. No information on the role of wild ungulates; infection is asymptomatic in blesbok (Damaliscus dorcas albifrons) Eland (Tragelaphus oryx) may act as a reservoir

A zoonosis Mentioned by many countries and stressed by some; complex situation because of the number of different serotypes Cuba Australia

Republic of Korea New Caledonia France

United Kingdom

Sweden

Rat and deer Feral pigs, feral cattle, water buffalo, deer and certain indigenous species, such as wombat Voles and rats Mice, timor deer Rodents, hedgehog (Erinaceus europaeus) Brown rat (Rattus norvegicus) and other wild species Hedgehog (Erinaceus europaeus)


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Q fever

Rabies

Anaplasmosis, babesiosis, toxoplasmosis and other protozoal infections

South Africa

France

Switzerland

Uganda

South Africa

Zambia

Zimbabwe USA Mexico

Bulgaria Switzerland USSR

South Africa

Australia Bulgaria Sweden

A zoonosis Tick-transmitted, perhaps with a wildlife cycle High serological prevalence in the roe deer (Capreolus capreolus) Game animals and small wild mammals act as reservoirs; roe deer (Capreolus capreolus) are involved directly

A zoonosis Stray dogs, black-backed jackal (Canis mesamelas) Stray dogs, yellow mongoose (Cynictis penicillata), black-backed jackal (Canis mesomelas), wild cats (Felis spp.), genet (Genetta), greater kudu (Tragelaphus strepsiceros), feral cat, ratel (Mellivora capensis), bat-eared fox (Otocyon megalotis), meercat (Suricata suricata). Rabies has been diagnosed in 36 wild species, of which the following have an epidemiological role: yellow mongoose, black-backed jackal, wild cat, genet, meercat, bat-eared fox and greater kudu Fox, jackal, ratel (Mellivora capensis), mongoose, etc. Stray dogs, jackals

Vampire bats (Desmodus rotundus) are responsible for paralytic rabies in cattle

Fox (Vulpes vulpes) Stray dogs, fox (Vulpes vulpes), golden jackal (Canis aureus), wolf (Canis lupus), raccoon-dog (Nyctereutes procyonoides)

Complex situation; toxoplasmosis associated with cats (a zoonosis)

Toxoplasmosis associated with feral cats

Toxoplasmosis in hares

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Country which Wildlife species Disease name provided and (when applicable)

information susceptibility of man

Paratuberculosis USA

Brucellosis

Tuberculosis

South Africa

Cuba USA

Mexico Australia Bulgaria France

Switzerland

USSR

South Africa

Zambia Cuba USA

Australia

A zoonosis African buffalo (Syncerus caffer), hippopotamus (Hippopotamus amphibius); wild animals are not reservoirs, but are infected by domestic animals Feral pigs Bison (Bison bison), wapiti (Cervus canadensis), white-tailed deer (Odocoileus virginianus), fur-bearing animals; feral pigs have been examined for brucellosis

Feral cattle and feral pigs

Hares (Lepus capensis) infected with Brucella suis Hares (Lepus capensis) introduced for repopulation, infected with Brucella suis Saiga (Saiga tatarica) infected with B. melitensis; hares (Lepus capensis), wild boar (Sus scrofa)

A zoonosis Wildlife infection from contact with man and domestic animals. Diagnosed in: African buffalo (Syncerus caffer), greater kudu (Tragelaphus strepsiceros), common duiker (Cephalophus grimmia), lechwe (Kobus leche); all isolates have been Mycobacterium bovis. M. bovis, M. avium and M. tuberculosis (human) have been isolated from many species kept in zoos, including monkeys and elephants Wild ruminants Diagnosed in zoos Axis deer, feral pigs, mongooses and wild goat are under surveillance on Molokai Island (Hawaii) Water buffalo, feral pigs and feral cattle; marsupials seem to be infected rarely


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Tuberculosis (contd.)

Taiwan R.O.C. Finland United Kingdom

Dermatophilosis (Senkobo skin disease)

Sweden Switzerland

USSR

South Africa

Infectious bovine rhinotracheitis

South Africa

Switzerland

Farmed deer Wild birds Badgers (Meles meles) act as wildlife reservoir for bovine tuberculosis (M. bovis), and 10% are infected in certain areas. In regions where badgers are present, roe deer (Capreolus capreolus) and sika (Sika nippon) may become infected; also red deer (Cervus elaphus) introduced into the country. M. bovis recovered from rat, fox (Vulpes vulpes), mole (Talpa europaea) and mink Birds a possible source of M. avium M. avium from pigeons and birds of prey. M. bovis has disappeared from game animals following eradication of the disease in cattle M. avium and M. bovis isolated from wild birds. Infection may be present among wild boar (Sus scrofa) and red deer (Cervus elaphus)

Occurs in eland (Tragelaphus oryx), giraffe (Giraffa camelopardalis), Thomson's gazelle (Gazella thomsoni), zebra (Hippotigris), greater kudu (Tragelaphus strepsiceros), roan antelope (Hippotragus equinus), sable antelope (Hippotragus niger). It is hard to discover the true source of infection

Specific antibodies occur in 14 wild species, including African buffalo (Syncerus caffer), eland (Tragelaphus oryx), brindled gnu (Connochaetes taurinus), common Waterbuck (Kobus ellipsiprymnus), reedbuck (Redunca spp.), hippopotamus (Hippopotamus amphibius). The virus has been isolated from gnu. See the comments in the chapter on herpesvirus infections Wild animals play no part in infecting domestic animals

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Theileriasis

Trichomoniasis

Trypanosomiasis

Venezuelan equine encephalomyelitis

Trichinellosis

South Africa Zimbabwe

Australia

Uganda

South Africa

Zambia

Zimbabwe

USA

Mexico

USA Bulgaria

Finland Portugal United Kingdom Sweden

Switzerland USSR

No comments received Theileria parva lawrenci in African buffalo (Syncerus caffer). Vectors are Rhipicephalus zambesiensis and R. appendiculatus

Occurs among feral cattle

A zoonosis Wild animals are a source of infection; tsetse fly vector Mainly T. congolense and T. vivax in cattle, T. brucei in horses and T. simiae in pigs. 60% of cases of infection are attributable to wild pigs and 35% to wild ruminants as follows: 10% for African buffalo (Syncerus caffer) and 25% for eland (Tragelaphus oryx), greater kudu (Tragelaphus strepsiceros) and bushbuck (Tragelaphus scriptus) combined; the African elephant (Loxodonta africana) accounts for only 5% Species encountered: T. congolense, T. vivax, T. brucei, T. zambesiensis

A zoonosis

Surveillance of wild birds and rodents was conducted in Texas in 1971

A zoonosis Feral pigs Brown bear (Ursus arctos) Wild boar (Sus scrofa) Wild carnivores Wild boar (Sus scrofa) Rat and fox (Vulpes vulpes) Fox (Vulpes vulpes) and badger (Meles meles) Fox (Vulpes vulpes) Reservoirs are: wolf (Canis lupus), fox (Vulpes vulpes), wild boar (Sus scrofa), badger (Meles meles),


7 1 5




Trichinellosis (contd.)

Duck virus enteritis

Psittacosis-ornithosis

Myxomatosis

Tularaemia

Leishmaniasis

USSR (contd.)

United Kingdom

France

United Kingdom

USSR

Australia France Portugal Switzerland

Bulgaria Finland USSR

South Africa

raccoon-dog (Nyctereutes procyonoides), bear (Ursus arctos), arctic fox (Alopex lagopus), marine mammals

Wild ducks, particularly mallard (Anas platyrhynchos)

A zoonosis

Psittacides in captivity: semi-domesticated pigeons (Columba livia) Wild birds infected; diagnosed in domestic ducks and turkeys Pigeons and sparrows

Rabbit destruction campaigns Wild rabbit (Oryctolagus cuniculus) Wild rabbit (Oryctolagus cuniculus) Wild rabbit (Oryctolagus cuniculus)

Hares (species not given) Common vole (Microtus arvalis), water vole (Arvicola amphibius), muskrat (Ondatra zibethicus)

A zoonosis Hyrax (Procaviidae)

OTHER DISEASES NOT LISTED IN THE TWO PREVIOUS CATEGORIES

Malignant South Africa catarrhal fever

With intensification of the rearing of game animals, this disease has become the most important cause of death of big game. Both white-tailed and brindled gnu (Connochaetes gnou, C. taurinus) act as asymptomatic carriers. The virus has also been isolated from red hartebeest (Alcelaphus buselaphus) and tsessebe (Damaliscus lunatus) but there is no evidence of transmission. All Cervidae and Bovidae are susceptible, excepting perhaps the African buffalo (Syncerus caffer).

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Malignant catarrhal fever (contd.)

Herpesvirus mammillitis (Allerton herpesvirus infection)

Ephemeral fever

Contagious ecthyma

Mange

Listeriosis

South Africa (contd.)

Zimbabwe Australia

South Africa

South Africa

Australia

Switzerland

Australia

Bulgaria

Finland Portugal Sweden

Australia

Finland USSR

Eland (Tragelaphus oryx) and giraffe have been infected experimentally. The European sheep-associated form also occurs Brindled gnu (Connochaetes taurinus) Imported deer living in the wild state

Known to occur in African buffalo (Syncerus caffer); virus isolated. A serological survey showed that nearly all buffalo were infected; antibodies also present in giraffe (Giraffa camelopardalis), Waterbuck (Kobus ellipsiprymnus), hippopotamus (Hippopotamus amphibius), eland (Tragelaphus oryx), oryx (Oryx gazella), impala (Aepyceros melampus), bushbuck (Tragelaphus scriptus) and gnu (Connochaetes spp.)

54% of African buffalo (Syncerus caffer) serologically positive, also 62% of Waterbuck (Kobus ellipsiprymnus), 9% of gnu (Connochaetes spp.) and 2.8% of red hartebeest (Alcelaphus buselaphus) Water buffalo, feral cattle and deer introduced into Australia

A zoonosis

Chamois (Rupicapra rupicapra)

A zoonosis Wombat, koala (Phascolarctos cinereus) and fox (Vulpes vulpes) Fox (Vulpes vulpes) and chamois (Rupicapra rupicapra) Fox (Vulpes vulpes) Fox (Vulpes vulpes) Fox (Vulpes vulpes)

A zoonosis Isolated from wild animals; sporadic cases among indigenous species (marsupials) Hares and wild birds Rodents (rodent-sheep cycle)

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Salmonelloses

Erysipelothrix infection

Enterotoxaemias

Verminous gastro-enteritis

Porcine parvovirus infection

USA

Australia

France Sweden

Australia

Bulgaria USSR

Bulgaria

Bulgaria

USSR

A zoonosis Small mammals and birds, infecting poultry flocks Isolated from wild animals; sporadic cases among indigenous species (marsupials) Sparrows Isolated from wild animals; only 3% of foxes infected

A zoonosis

Isolated from wild animals; sporadic cases among indigenous species (marsupials)

Rodents, birds and wild boar {Susscrofa)

Losses among fallow deer (Dama dama) and red deer (Cervus elaphus)

Has reduced populations of red deer (Cervus elaphus)


S P E C I F I C I T Y O F I N F E C T I O N S A N D I N F E S T A T I O N S

The specificity of infections and infestations is very well illustrated by the herpesvirus infections in wild ruminants , by Dictyocaulus spp. infestations in deer and by the special case of infections among the wild fauna of Australia.

The specificity of herpesvirus infections in domestic and wild ruminants

Serological surveys have shown for some years (145) that numerous species of wild animals possess specific antibodies which neutralise infectious bovine rhinotracheitis (IBR) herpesvirus (Bovine herpesvirus 1). A list of such species is given in Table II .

It has been found only recently that species other than cattle can become infected with a virus antigenically related to , but distinct from Bovine herpesvirus 1. An initial investigation (serological survey) suggested that other species can become infected by the bovine virus, whereas subsequent and more thorough testing has demonstrated

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that they are, in fact, infected with a similar virus which is specific for them. Thus goats were stated to be susceptible to IBR virus as a result of serological tests. In fact, this species is most often infected by a herpesvirus of its own, Caprine herpesvirus 2 (2, 44). Experimental infection of goats with Bovine herpesvirus 1 produces no more than a mild infection, and the bovine virus fails to establish a latent infection, indicating a lack of true adaptat ion (99).

A similar situation probably exists in the non-domesticated species which react serologically to Bovine herpesvirus 1. Three other herpesviruses related antigenically

T A B L E II

Range of susceptibility to infectious bovine rhinotracheitis virus and antigenically related viruses

Family Subfamily Species

Cervidae Cervinae Red deer (Cervus elaphus) Eastern wapiti (Cervus canadensis)

Odocoilinae Roe deer (Capreolus capreolus) White-tailed deer (Odocoileus virginianus) Mule deer (Odocoileus hemionus) Elk (Alces alces)

Rangiferinae Reindeer (Rangifer tarandus) Caribou (Rangifer tarandus caribou)

Giraffidae Giraffinae Giraffe (Giraffa camelopardalis)

Antilocapridae Pronghorn (Antilocapra americana)

Bovidae Tragelaphinae Eland (Taurotragus oryx) Greater kudu (Tragelaphus strepsiceros)

Bovinae Domestic ox (Bos taurus) Asian buffalo (Bubalus arnee) African buffalo (Syncerus caffer)

Alcelaphinae Red hartebeest (Alcelaphus buselaphus) Tsessebe (Damaliscus lunatus) Blesbok (Damaliscus dorcas) White-tailed gnu (Connochaetes gnou) Brindled gnu (Connochaetes taurinus)

Hippotraginae Roan antelope (Hippotragus equinus) Sable antelope (Hippotragus niger) Addax (Addax nasomaculatus)

Reduncinae Common Waterhuck (Kobus ellipsiprymnus) Kob (Kobus kob) Lechwe (Kobus leche) Southern reedbuck (Redunca arundinum) Bohar reedbuck (Redunca redunca)

Antilopinae Thomson's gazelle (Gazella thomsoni) Springbok (Antidorcas marsupialis) Tmpala (Aepyceros melampus)

Caprinae Chamois (Rupicapra rupicapra) Domestic goat (Capra aegagrus hircus)

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to Bovine herpesvirus 1 have been isolated recently: type 1 herpesvirus of Cervidae (55, 143), a herpesvirus of reindeer (Rangifer tarandus) (32, 33) and one of the Indian buffalo (Bubalus arnee). The case of infection with cervid herpesvirus, isolated from Cervus elaphus, provides a good example. Earlier serological surveys had revealed antibodies specific for Bovine herpesvirus 1 in this species (63, 64), whereas recently a herpesvirus of deer, antigenically related to the former virus, has been isolated (55) from cases of conjunctivitis among fawns reared in Scotland. The frequency of this infection varies according to particular circumstances, for the percentage of serological conversions was 2 9 % in Great Britain (82) and only 1 1 % in Belgium (143, 145). Specificity of the virus has been demonstrated (118), for deer could be infected with their own virus, which remained latent after a primary infection, while infection with the bovine virus failed (123). Conversely, when the bovine virus did multiply in deer, the infection remained mild. The situation in deer is similar to that in goats, and it is probable that every case of serological conversion in deer is attr ibutable to the cervid virus.

A remarkable finding is that , while the bovine virus can produce a moderate infection in deer, the converse does not apply, and deer present no risk for cattle.

Unfortunately, s tandard serological tests cannot distinguish the two types of infection in deer, so they have been wrongly regarded as a potential source of infection of cattle with Bovine herpesvirus 1.

More precise techniques capable of distinguishing the two types of infection have now become available (2), but they are difficult to apply.

A situation similar to that in deer may well exist in reindeer (Rangifer tarandus). Earlier serological surveys showed that 2 3 % of reindeer and a certain percentage of caribous possessed antibodies to Bovine herpesvirus I (32, 34). A reindeer herpesvirus has recently been isolated (33), though experimental inoculation did not produce any symptoms in reindeer. This virus proved, however, to be pathogenic for cattle (84).

The situation in America is probably similar to that in Europe (22, 62). In Africa it is rather more complex, judging from the very high prevalence of antibodies to Bovine herpesvirus 1 observed in African buffalo (Syncerus caffer), eland (Taurotragus oryx) and gnu (Connochaetes spp.) (47). Bovine herpesvirus 1 has been isolated from gnu (59, 76, 75), though the only lesion observed was that of vulvovaginitis. Maré (67) was unable to reproduce this disease in elands.

Apar t from African buffalo (the susceptibility of which does not seem to have been elucidated), the gnu species is the only one known to be susceptible to Bovine herpesvirus 1. The infection remains confined to the genital tract, and it seems improbable that the infection would spread to other species, because of its sexual transmission. Herpesviruses can persist latently in small populat ions of animals without infection from outside (92, 88, 91 , 141). It therefore seems reasonable to assume that other African species of wild ruminants , serologically positive to Bovine herpesvirus 1, are infected with their own types of virus.

The problem of infection with bovine mammillitis herpesvirus (Bovine herpesvirus 2) is rather different. It is known that in cattle, from which the virus has been isolated, the virus remains latent, and the infection is seldom manifested in the clinical form (83).

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In Africa, many species have shown serological evidence of infection with this virus (Table III) (104, 7 1 , 106, 41).

T A B L E III

Range of susceptibility to bovine mammillitis herpesvirus or antigenically related viruses

Family Subfamily Species

Giraffidae Giraffinae Giraffe (Giraffa camelopardalis)

Bovidae Tragelaphinae Greater kudu (Tragelaphus strepsiceros) Bushbuck (Tragelaphus scriptus) Eland (Taurotragus oryx)

Bovinae Domestic ox (Bos taurus) African buffalo (Syncerus caffer)

Alcelaphinae Red hartebeest (Alcelaphus buselaphus) Tsessebe (Damaliscus lunatus) Brindled gnu (Connochaetes taurinus)

Hippotraginae Roan antelope (Hippotragus equinus) Sable antelope (Hippotragus niger) Gemsbok (Oryx gazella) Beisa oryx (Oryx beisa)

Reduncinae Common waterbuck (Kobus ellipsiprymnus) Southern reedbuck (Redunca arundinum) Defassa waterbuck (Kobus defassa)

Antilopinae Springbok (Antidorcas marsupialis) Impala (Aepyceros melampus)

Caprinae Domestic goat (Capra aegagrus hircus) Domestic sheep (Ovis ammon aries)

Although the virus has been isolated from African cattle (54) with a disease resembling lumpy skin disease, it has not as yet been isolated from wild animals, with the exception of the African buffalo (Syncerus caffer) (58, 106), which is particularly close to the domesticated species.

Infection of wild species with Bovine herpesvirus 4 is not mentioned in the reports. A n investigation in France and Belgium failed to find wild ruminants that were serologically positive (144), although 2 2 % of Belgian cattle were positive.

Such a difference between domestic and wild animals is quite common. For example, in Belgium the percentage of wild animals serologically positive to Bovine herpesvirus 1 is very small (143) even though it is a major pathogen of cattle. The opposite situation occurs in Finland, where the infection is absent from cattle despite positive tests in reindeer. This is another observation to confirm the rarity of transfer of herpesvirus infections from wild species to cattle, and vice versa, either because of lack of contact between the two types of animals (particularly under conditions of intensive husbandry) or for purely biological reasons, such as a specificity of the infections and particular modes of transmission (e.g. sexual).

The special case of malignant catarrhal fever will be dealt with below.

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The specificity of Dictyocaulus infestations

A question is often raised concerning the threat posed by wild Cervidae as a reservoir of Dictyocaulus species pathogenic for cattle.

An investigation conducted recently in the United Kingdom (13) showed that fallow deer (Dama dama) did not act as a reservoir of Dictyocaulus for cattle.

The possible role of red deer (Cervus elaphus) as a reservoir of bovine species of Dictyocaulus has been questioned.

Studies of red deer reared for venison in the United Kingdom have shown that this deer harbours a Dictyocaulus sp. different from D. viviparus, which is responsible for parasitic bronchitis in cattle (74), although no difference is detectable between the two species by the usual morphological examination. Consequently, deer are not reservoirs of nematodes pathogenic for cattle.

Susceptibility of marsupials to infections of placental mammals

The Australian continent is a special and exceptional case.

Before the white man arrived, the only placental mammals on the continent were human beings, dingoes (commensal with human beings), bats , rodents and coastal aquatic mammals . The arrival of the white m a n coincided with the introduct ion of numerous other species of placental mammals , some of which returned to their wild state: rabbit (Oryctolagus cuniculus), fox (Vulpes vulpes), water buffalo, cattle, pig, dromedary, horse and donkey.

Although there is little information on the susceptibility of the indigenous mammals to infections and infestations of introduced placental mammals , the report from Australia clearly suggests that problems of cross-contamination (from wild or feral species to domesticated species) have arisen from the introduced domestic animals that have returned to the wild state.

This shows rather well that the phylogenic distance between eutherian mammals and marsupials acts as a good barrier to cross-infection (existence of a refractory state).

The case of ornithosis-psittacosis (chlamydia infection)

This disease further illustrates the errors of interpretation which may arise from a serological survey of wild or feral species. Many of the reports have emphasised the risk posed by the feral pigeon (or rock dove, Columba livid) in transmitt ing ornithosis to human beings.

Such statements are often based on the results of serological testing, which show a high proport ion of serological conversions in these birds (38).

An investigation in Belgium (151) has shown that no serologically positive pigeon was excreting Chlamydia psittaci, confirming observations by Lüthgen in 1971 (66) of a complete lack of agreement between the elimination of Chlamydia psittaci by semi-domesticated pigeons and the titre of complement-fixing antibody in their serum. This is confirmed by the absence of infection among pigeon fanciers, who constitute the human populat ion at greatest risk.

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In fact, only psittacine birds pose a real threat . The reason for the discordance in pigeons between the high percentage of serological conversion and the absence of pathogen excretion may be explained by a different biology of the infection in this species, since Chlamydia psittaci can be isolated from viscera (148).

RISKS T O W I L D A N I M A L S C R E A T E D B Y D O M E S T I C A N I M A L S

The epidemiological links between domestic and wild species in the transmission of certain diseases are often considered from a single direction only, and so there may be a failure to appreciate the risks to wild species posed by domestic species.

But this situation may also apply. The most striking example of infection of wild species by domestic species is rinderpest, and one may also mention brucellosis and tuberculosis.

Rinderpest

There can be no doubt that rinderpest is the most dangerous disease of cattle at present (108). Of Asiatic origin, it has decimated European herds during periods of upheaval (such as wars). Complete eradication was achieved at the end of the last century, apart from a brief reappearance in Belgium in 1920 (7, 90) and in the Rome Zoo in 1949 (24).

Until the last century, Egypt was the only African country to be infected periodically. But in about 1880, on the occasion of the first Italian expedition to Abyssinia, rinderpest spread along the Nile and thence to the entire African continent, with the exception of Nor th Africa, which is protected by the barrier of the Sahara Desert (89). The history of rinderpest in Africa is therefore relatively recent.

The introduction of rinderpest by domestic cattle had severe effects on big game. As Table I shows, practically every species of the order Artiodactyla is probably susceptible to rinderpest virus, while the most susceptible species belong to the Ruminant ia and Suidae (102).

The wild animals originally infected by domestic animais were regarded for decades as the reservoir of infection. They were invariably incriminated each time an outbreak occurred among cattle. For this reason, control of the disease in East Africa (Tanzania and Zambia) entailed the killing of more than 10,000 wild ruminants between 1941 and 1951. In fact, because certain wild species are very susceptible to this disease, the appearance of rinderpest among wildlife may provide the first indication of the presence of the disease in a given region.

In the past it was generally recognised that large concentrations of wild animals, as in the Serengeti region of East Africa, could act as " long-term reservoirs" of the virus, in the absence of the disease among cattle (111). This concept, still held by some workers, is based essentially on the discovery of specific antibodies in wild animals (126). Even if this discovery is confirmed, it does not constitute sufficient proof that wild species act as a reservoir of the virus (110).

In fact, a high frequency of antibodies in certain species may indicate merely that certain individuals of the species have become immune to the disease (it is known

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that cattle which survive the disease acquire a solid and durable immunity). The question of specificity of the reactions was raised again recently, when antibodies to rinderpest virus were detected among cattle in New Caledonia, where the disease does not exist (Provost, personal communicat ion) .

Fur thermore, there is a good argument against wild animals acting as a reservoir of rinderpest. Elimination of the disease from cattle in South Africa following the panzootic of 1888-1901 and in the Serengeti region of Tanzania between 1968 and 1970 was followed in each case by a diminution in the occurrence of neutralising antibody in the wildlife populat ion, which remained very dense in both regions (108). This seems to suggest that the disease may not occur among the wild animals of a given region unless it is also occurring among domestic animals. Wild animals would not therefore constitute a reservoir of rinderpest, and their role would be confined to disseminating the disease by sporadic contact with domestic animals in an enzootic or epizootic situation (107).

The question of the possible role of wild species in rinderpest is of major importance, because it partly governs the success of the vaccination campaigns being conducted at present on African cattle (112).

Pest of small ruminants has never been reported among wild animals, al though an outbreak has been reported recently from a zoo at Al Ain, affecting representatives of Gazellinae and Caprinae, also a member of Hippotraginae and possibly of Tragelaphinae as well (37).

Brucellosis

Bovine brucellosis is another disease which has led to controversy about the possible role of wild animals as a reservoir of infection. The problem arises mainly in European countries trying to eradicate the disease. A serological survey in France showed that only 2 of 54 red deer (Cervus elaphus) and none of 696 roe deer (Capreolus capreolus) possessed specific antibodies (12), so that wild Cervidae do not seem to be involved in the transmission of bovine brucellosis (69). It is probable that domestic animals are responsible for infecting wild animals, and not vice versa, as demonstrated in South Africa by the finding of brucellosis in African buffalo (Syncerus caffer) and hippopotamus (Hippopotamus amphibius).

In the same way, bison (Bison bison) and Cervidae have become infected in the USA.

Many European countries report the frequent occurrence of Brucella suis infection among hares (Lepus capensis), following the observations of Witte (159), but without being able to establish an epidemiological link with the infection in pigs. As a consequence of the intensive husbandry of pigs, they have little possibility of contact with hares.

Tuberculosis

There are numerous instances of inadvertent infection with mycobacteria, particularly in species of wild animals kept in captivity in zoos, where they are exposed to human infection. In South Africa tuberculosis has been diagnosed in many wild species, including African buffalo (Syncerus caffer), greater kudu (Tragelaphus strepsiceros), common duiker (Cephalophus (Sylvicapra) grimmia) and lechwe (Kobus leche), from all of which Mycobacterium bovis was isolated. These cases resulted from wild animals coming into contact with human beings or domestic animals.

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In Switzerland, M. bovis infection disappeared from game animals following its eradication from cattle.

Roe deer (Capreolus capreolus) captured in France have all been serologically negative.

A special situation apparently occurs in the United Kingdom, where the badger (Meles meles) constitutes a wildlife reservoir of bovine tuberculosis (9). M. bovis has been detected in 10% of badgers. In 1986, 4 3 % of the fresh outbreaks of tuberculosis among cattle were attributed to infection from badgers (155, 156, 157).

This problem is particularly serious in South-West England, where badgers were responsible for 6 5 % of outbreaks among cattle confirmed during 1986. There is a high density of badgers in this region, in some places reaching 20 individuals per square kilometre. Infected badgers excrete tubercle bacteria in their expectorations, faeces, urine and in the pus of bite wounds. Apar t from badgers, no other wild species seems to be involved in transmitting the disease to cattle. In regions where infected badgers are found, there have been cases of tuberculosis in roe deer (Capreolus capreolus) and sika deer (Cervus nippon). Red deer (Cervus elaphus) imported from Czechoslovakia have also shown a high incidence of tuberculosis. The role of the avian tubercle bacterium has yet to be established (27).

Because of the decisive role of badgers in transmitting tuberculosis to cattle, the authorities have taken steps to reduce the badger populat ion in certain areas, and are investigating an efficacious method of vaccinating them.

Conclusions

These examples show that the problem of epidemiological links between domestic and wild animals must not be considered to occur just in one direction, and that certain infections can disappear from wildlife when they are absent from domestic animals.

In some cases it may be better justified to protect wild species from contact with domestic animals than the reverse, particularly when the wild species are of economic importance.

C U L T U R A L A N D E C O N O M I C R O L E O F T H E F A U N A

The cultural and economic role of the fauna has changed considerably over the last years in line with the way in which it is perceived by the general public, particularly in developed countries. To an increasing extent the fauna is regarded not as a competitor to the species reared by man , but as a complement, a resource to be preserved, managed and developed (73, 129).

Long-standing attitudes regarding the use or destruction of wildlife resources must now take into account the growing importance of environmental and conservational viewpoints. The situation has changed in favour of rights for wild animals more or less comparable to those of domestic animals. In addition, in many cases the wild species have acquired an economic importance by involvement in recreation or as a source of human food, and so they deserve to be treated in a way similar to domestic animals.

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Such changes in human attitudes to the larger wild animals have their influence on the way in which epidemiological links between domestic and wild species are perceived and managed. They also affect the way in which the animals are managed.

Each change in cultural or food utilisation modifies the ecology of infections and the host-parasite relationships, as well as possible relationships to domestic animals. The situations which arise as a consequence can be classified as follows: national parks and protected species; zoos and game parks; game ranches and farms; the rearing of wild animals for repopulat ion.

National parks and protected species

In national parks the wild species are in an exceptionally favourable position, being protected theoretically from the incursion of domestic species. The initial ecological system is usually respected, and contacts with domestic species are practically nil. In some cases there may be human intervention concerning the health status of certain rare species. For example, in South Africa roan antelopes are systematically vaccinated against anthrax.

The situation may not always be as clear, however. The type of relationship between domestic animals and big game, particularly in African countries, varies with the type of land use (120).

Land may be used for grazing by domestic animals, or may form par t of game reserves and national parks for use by the wild fauna. Because of the dominance of t ranshumant husbandry in Africa it is obvious that there is more chance here than elsewhere of contact between domestic and wild animals.

Interrelationships among wild animals, domestic animals and the environment may be summarised as follows:

a) On grazing land: - competition for feed between wild and domestic animals; - predation of domestic animals by wild carnivores; - erosion produced by the wildlife alone or in association with domestic stock; - role of wild animals as reservoirs of diseases of domestic animals.

b) In the reserves: - domestic animals may change the environment t o the detriment of wildlife; - erosion produced by domestic animals alone or in association with the fauna,

to the detriment of the wild habitat; - domestic animals compete with wild animals for water and other needs.

Along with this list of unfavourable effects, it should be pointed out that cohabitation between domestic and wild species may also have some beneficial effects, provided that the proport ions of the two groups are carefully regulated, and that they are complementary in feeding habits.

Zoos and game parks

These are also a quite special case because they unite within an enclosed and restricted area a collection varying in numbers and species, coming from very different

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origins. The building up of a collection will draw on animals of unknown health status, captured in their country of origin. As a consequence, zoos may provide ideal conditions for the sharing of certain infections, and there have been some regrettably spectacular incidents, such as the introduction of rinderpest into the Rome Zoo in 1949, also the appearance of the African form of malignant catarrhal fever in a European bison (Bos bonasus) in a Dutch zoo (139), and in the San Diego Zoo among gaur (Bos gaurus), swamp deer (Cervus duvauceli) and banteng (Bos javanicus) (45). There was likewise the recent and dramatic introduction of African horse sickness into Spain by zebras from Namibia which were destined for safari parks (121). Because of their isolation and special nature, however, zoos are only exceptionally a source of infection to domestic stock in their vicinity.

Game ranches and farms

In many cases, wild species can provide a better renewable source of animal protein than domesticated species, particularly in Africa, where the natural ecological systems are complex and often very fragile. Wild species may succeed better than domestic species in utilising the available plant resources, thereby enhancing productivity. Such considerations have resulted in the establishment of ranches and farms for rearing certain wild species.

This practice has developed considerably in certain African countries, such as Zimbabwe. As a consequence, many cattle farmers no longer see game animals as pests to be exterminated because they compete with domesticated species, but rather as an important source of income. In ranching systems, cattle and game animals may be reared together, apparently without creating any particular health problem. Some breeders prefer to keep them separate, with the wild animals inside enclosures to prevent contact. By contrast, cattle may be kept within enclosures to protect them from contact with certain wild species such as the African buffalo, when this creates a particular problem.

Such evolutions in husbandry practices should automatically engender new approaches to health problems, including the study of the infections specific to wild species, and those shared with domesticated species. Another approach has been to form herds of wild species exempt from certain infections, like the herds of African buffalo (Syncerus caffer) in Zimbabwe which are exempt from foot and mouth disease.

Similar patterns may be seen in Europe and New Zealand where deer farming, particularly of red deer (Cervus elaphus) and fallow deer (Dama dama), has become an important activity. Red deer are reared on a large scale in the United Kingdom, particularly in Scotland, for venison. Deer have proved to be a better source of income for the farmer than sheep, the animal traditionally reared in the regions. The farming of these species at high density has led to the emergence of new health problems which must be investigated. Malignant catarrhal fever is the major cause of mortality beyond a certain age (114, 143). Repeated contact with sheep is the main source of infection.

The existence of deer farms should lead to a reconsideration of the problem of potential exchanges of infections with domesticated species, but once again in bo th directions.

Animals for repopulation

Certain species of game have become rare, particularly in Europe, and this has led to the creation of premises for repopulation, or the introduction of animals from other countries better supplied with the species.

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These practices have not always been accompanied by adequate disease control precautions, particularly since the animals tolerate their temporary captivity very poorly, and are therefore transported and released quickly.

Certain countries have thus complained that animals for repopulation have been responsible for introducing disease into the indigenous fauna, with subsequent transmission to domestic animals. In Switzerland, for example, Brucella suis has been found in hares introduced for repopulat ion.

It would clearly be desirable to be more vigilant about the health status of wild animals reintroduced into a natural ecological system, for premises where the animals are gathered together favour the exchange of infections between animals of the same species.

Conclusion

The cultural and economic use of wild species creates new health problems, not only with respect to the possible infection of domestic animals, but also in regard to the improvement of living conditions of wild species in their natural surroundings, or under the conditions of some form of farming.

H E A L T H M A N A G E M E N T O F T H E W I L D F A U N A I N T H E N A T U R A L E N V I R O N M E N T

The new economic and cultural values attached to wild species have altered the conception of health problems as well as veterinary attitudes towards them.

Whereas considerable progress has been made in the control of diseases of domesticated animals, there has not been nearly the same interest in infections and infestations of wild species (128).

Particularly in Africa, veterinarians have incriminated wildlife as a source of diseases of livestock, often without actual scientific proof. A widely held opinion maintained that it was futile to study wild species, because their diseases could be overcome automatically by destroying them or reducing their numbers . Because of this attitude, many research workers were prevented from conducting systematic and well-organised research into the infections and infestations of wild species. Indeed, such studies were often regarded as superfluous.

Some of these obstacles have now been lifted, and efforts are being made to intervene and manage the health problems of wild animals, either to improve the health of the animals or to prevent possible transmission of a given disease to other wild species, to domestic animals, or to man .

Examples of such intervention involve the treatment of parasitoses of Cervidae, and vaccination of European foxes against rabies.

Health management

The first problem raised by health management for wild species in their natural surroundings is that of access to the animals.

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Under exceptional circumstances, such as the case of rare species in South African national parks, individual animals may be handled in order to vaccinate them against anthrax. In most cases, however, the preferred form of treatment is indirect. This has long been the practice in Europe for the control of the parasitic burden of deer, which receive appropriate oral medication. Examples of such treatment have been cited by Bulgaria.

Vaccinating foxes against rabies by the oral route

A notable example of preventive health intervention in the natural environment is provided by the control of fox rabies in Europe. Contrary to the situation in regions of Africa, America and Asia, the epidemiology of terrestrial rabies in Europe is relatively simple, for the red fox (Vulpes vulpes) is the principal reservoir and vector (3). Attempts have been made to vaccinate wild animals against rabies for more than twenty years (11).

The objectives of this prophylactic procedure are fundamentally the same as in hygienic prophylaxis, except that instead of destroying the virus vector, the animals are rendered refractory to infection. Following a report by Andra l and Blancou (6), the OIE is insisting on guarantees that the procedure shall be innocuous for bo th target and non-target species.

The first criterion which any vaccination has to comply with is efficacy.

Experiments conducted with attenuated strains of rabies virus have shown that strain SAD/B19 , developed at the Tübingen Institute in Germany, is fully effective in an adequate titre (16). The age of the animal at the time of vaccination is important , for adult foxes respond better than young ones.

The results of field trials of vaccination, conducted for the first time in Switzerland (136, 137) and then in the Federal Republic of Germany (135) and other European countries (93, 36, 10, 18) have been very promising.

Between 65 and 7 5 % of foxes in a given region can be immunised by distributing bait containing the vaccine. Other species which may compete with foxes in eating the bait are badgers (Melesmeles), wi ldboar (Susscrofa) and certain small mammals (57).

A new way of vaccinating foxes against rabies by the oral route has been opened up with a vaccine containing recombinant vaccinia-rabies viruses, obtained by genetic manipulation (61); Wiktor et al. (154) have already shown its efficacy.

This recombinant virus is perfectly efficacious and harmless for foxes, the target species for vaccination in nature (17).

It is also safe for all non-target species tested so far, including badgers (Meies meles) and wild boar (Sus scrofa), the principal competitors for taking bait (94).

Moreover, the recombinant virus is suitable for immunising young foxes (19).

The first field trial with recombinant virus vaccine was conducted in Belgium on 24 and 25 October 1987 (95).

The long-term consequences of vaccinating foxes against rabies have yet to be evaluated, for vaccination is giving rise to a novel situation in nature , that of a populat ion immune to a disease which formerly took a practically inexorable course.

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S O M E S P E C I A L C A S E S

Whereas the preceding chapters have concentrated on the general epidemiological links between wildlife and domestic animals, the chapter which follows will describe some special situations selected because of their importance, namely, malignant catarrhal fever in Africa, African swine fever, foot and mouth disease in African buffalo (Syncerus caffer), African horse sickness and pestivirus infections.

The African form of malignant catarrhal fever (MCF)

There are two forms of the disease, the African form associated with gnu and caused by Alcelaphine herpesvirus 1 (AHV-1), and the European form associated with sheep, the virus of which has not yet been identified (although it is probably a herpesvirus related to AHV-1) (109).

The gnu-associated form is obviously encountered in Africa. Neutralising antibody to AHV-1 is commonly found in members of the subfamily Alcelaphinae: the gnus (Connochaetes taurinus and C. gnu), red hartebeest (Alcelaphus buselaphus), topi or tsessebe (Damaliscus lunatus) and a member of the Hippotraginae, the beisa oryx (Oryx beisa) (116, 113).

The virus has been isolated from gnu (100, 106), and similar strains of virus have been obtained from hartebeest and topi (78). The topi virus does not seem to be pathogenic for cattle, because so far no case of M C F has been associated with contact with topis, and inoculation of cattle with topi virus does not reproduce the disease.

The mode of transmission between gnu and from gnu to cattle has been only partly elucidated. Stress at the end of gestation and at calving may reactivate a latent infection (130). In fact, a link between M C F in cattle and parturi t ion in gnu has been known for some time.

A fetal gnu may acquire infection within the uterus (101), al though the virus has not yet been demonstrated in fetal fluids and the placenta (127). Mushi et al. (77) have suggested that the virus multiplies in gnu and is excreted in nasal and ocular secretions (130) until 3-5 months of age. Progressive development of active immunity is probably responsible for the arrest of excretion (78).

Young, infected gnu can transmit the infection to their contemporaries. By the time they are one-year-old, most gnu have already been exposed to infection. This phenomenon is the origin of horizontal transmission of the virus between gnu and from gnu to cattle (79).

Although the virus can persist in gnu without provoking the disease, it is the in-contact cattle that develop the typical form of M C F . And unlike the gnu, a bovine is an epidemiological cul-de-sac, for there is no transmission by contact with cattle.

This lack of transmission may be due to the occurrence of the virus inside cattle in cell-associated form, whereas in gnu it is excreted in the free form. Thus the virus is well adapted to gnu, and infection of cattle is accidental.

These epidemiological features explain why, with the development of game farms in South Africa, gnu-associated M C F has become the main cause of mortality among cattle resulting from contact with the fauna.

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In cattle the disease occurs in March and April, 3-4 months after the calving season of gnu, the delay corresponding to the incubation period. Another peak occurs in September-October and has yet to be explained.

The European sheep-associated form of M C F is caused by a virus which has not yet been fully identified (116). This form of the disease may coexist with the other form in African countries which breed sheep, such as South Africa, and the two forms cannot be distinguished clinically.

It is likely that cattle become infected by contact with infected sheep in an inapparent manner , although cases of M C F have been described in which there was no direct contact with sheep (68, 160).

The indirect immunofluorescence test with AHV-1 antigen has revealed specific antibodies in a high proportion of serum samples, even those from specific-pathogen-free lambs (SPF) (125). It is therefore probable that many viruses related antigenically to AHV-1 occur in ruminants , particularly Caprinae, and are capable of producing subclinical infections.

Whenever the virus passes the species barrier to infect cattle or deer, it becomes pathogenic for these unadapted, unnatural hosts (Reid, personal communicat ion) .

As mentioned above, deer are particularly susceptible to M C F , the disease having been first described in 1961 in a Père David deer (Elaphurus davidianus) (53); this infection may have originated from gnu or sheep (115). Père David deer seem to be the species most susceptible to M C F (119). Cervidae are susceptible to both sheep-associated and gnu-associated forms of the disease (134, 153, 114).

Whereas M C F occurs only sporadically among cattle, in deer it may occur in epizootic form, involving a large number of animals. As early as 1906, Lupke described the decimation of a herd of spotted deer (or chital, Axis axis) by a disease which was probably M C F (114). Among indigenous species, the disease has been described in red deer (Cervus elaphus) of Europe (114); also in the mule deer (Cervus hemionus) (97) of Nor th America and in white-tailed deer (Odocoileus virginianus) (160). In Australia, New Zealand and the United Kingdom, where deer farming has become an important part of the livestock industry, M C F is regarded as a major disease problem. In cases which have occurred in New Zealand there has been no contact with sheep, and it has been suggested that a deer/deer cycle may occur, or that a reservoir host other than sheep may exist (68).

African swine fever (ASF)

This disease is of considerable economic importance (132, 133). Morbidity and mortality rates are very high, and may reach 100% during a primary infection. At present ASF occurs in an endemic state in many African countries south of the Sahara and, outside Africa, in Spain, Portugal and Italy (Sardinia). Its area of distribution is still expanding, and it makes brief incursions into territory outside its natural zone of extension, such as Belgium (132, 14) and the Netherlands.

Domestic pigs (Sus scrofa domestica) and wild boar (Sus scrofa) are among the species susceptible to ASF virus, and they are the only species to develop overt disease. Wild African Suidae such as the warthog (Phacochoerus aethiopicus), bush pig (Potamochoerus porcus) and giant forest hog (Hylochoerus meinertzhageni) are equally susceptible, but the infection is inapparent , and these animals act solely as

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asymptomatic carriers of the virus (51, 52, 103). Soft ticks of the genus Ornithodoros are susceptible to the virus and constitute a reservoir and biological vector.

The area of distribution of wild Suidae in Africa, particularly warthogs, is extensive south of the Sahara, and carriers of ASF virus have been detected in at least ten African countries (158). The free-range rearing of pigs, extensive in intertropical Africa, favours contacts between pigs and the natural reservoirs of the virus. In Africa there is often a relationship between the presence of the disease in pigs and its presence in wild Suidae, though this is not invariably the case. For example, in South Africa there is a relationship between wild Suidae possessing antibodies to the virus and the occurrence of vector ticks (98), but in East Africa this does not always apply (105). Warthogs infected when young seem to remain carriers of the virus in their tissues for a long time, probably for life, but only young animals develop viraemia with excretion of virus (158). N o proof has been obtained so far of virus transmission by contact between carrier warthogs and susceptible pigs (105).

While attempts to transmit ASF virus from wild Suidae to pigs by simple contact under experimental conditions have failed, it is well established that ticks can transmit the virus when they feed on pigs. Tick bites may be the origin of most pr imary infections of pigs in Africa (103). There is also a cycle of virus transmission between soft ticks (reservoir and vector) and warthogs (reservoir) during their period of parturi t ion. The existence of such a mode of virus conservation, independent of the principal species affected (pig), may explain the appearance of ASF among pigs after many years of absence.

Whereas adult wild African Suidae do not excrete the virus and do not transmit it among themselves, the same does not apply to domestic pigs, for the virus has been detected in excretions and secretions, and it is easy to produce direct transmission from one individual to another .

Taking into account the epidemiology of the disease, it should be possible to prevent transmission of the disease from the wild reservoir to the domestic pig by applying intensive husbandry methods coupled with strict observance of disease control precautions.

Foot and moutb disease (FMD) in Africa

The list of species susceptible to F M D is very long, with most of them belonging to the Artiodactyla (49, 131), as shown by the list of susceptible African species (Table IV). The most susceptible of African species is the African buffalo, Syncerus caffer (20).

In order to establish the role played by the fauna in the persistence and dissemination of F M D , it is necessary to find answers to the following questions (5):

a) Which species are receptive to the virus ? b) Do these animals become ill and excrete a large quantity of virus ? c) Which species become carriers of virus after a primary infection? d) Are wild animals carrying the virus capable of transmitting it to other animals,

particularly domestic animals ?

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Almost 70 species of mammals belonging to more than 20 families are receptive to natural or experimental infection with aphthovirus. There is considerable variation among species in the degree of susceptibility. Whereas the African buffalo (Syncerus caffer) and gnu rarely develop the clinical disease, greater kudu (Tragelaphus strepsiceros), impala (Aepyceros melampus), warthog (Phacochoerus aethiopicus) and bush pig (Potamochoerus porcus) may develop severe clinical disease following infection with aphthovirus (46).

Asymptomatic carriage of aphthovirus has been demonstrated in African buffalo (Syncerus caffer) and greater kudu (Tragelaphus strepsiceros).

African buffalo can continue to carry the virus for more than five years (25), and the kudu for at least 140 days (46). Bovines which have recovered from the disease can also carry the virus for long periods but , apart from these three groups, the other species do not seem to become carriers. Thus the impala (Aepyceros melampus), which is very susceptible to infection, does not carry the virus for long.

The question of transmission of aphthovirus by wild carriers to cattle remains controversial.

Condy and Hedger (25) placed susceptible cattle into close contact with African buffalo which were asymptomatic carriers for 2.5 years, during which t ime no cattle became infected. This result is surprising in view of the ease with which contact transmission normally occurs (29, 30). But the same authors have also obtained some contradictory results (50). One may conclude that the infection of cattle by wild animals carrying the virus is a rare event. It does seem that the African buffalo (Syncerus caffer) and to a lesser extent the greater kudu (Tragelaphus strepsiceros) play an important role in the persistence of aphthovirus in Africa within their own populations, but without transferring it to domestic animals. The main characteristics of the disease in buffalo are as follows (4): calves lose their passive immunity at 3-7 months of age and then become susceptible to infection. The staggering of births means that there are always some individuals becoming susceptible. The source of infection is either an adult carrier or an individual of the same age class with a primary infection, excreting virus in amounts similar to those excreted by domestic cattle, but for a longer period.

The result is that by three years of age, more than 80% of buffalo will have been exposed to the three SAT types of the virus.

The present state of knowledge does not permit conclusions to be drawn on the role of wild species, particularly African buffalo, in the transmission of F M D to domestic animals in Africa, particularly when the wide variability of strains is taken into account (20).

The role of the wild fauna, such as Cervidae in Europe, seems to be even more limited (23).

A serological survey conducted recently in France (12) revealed one red deer (Cervus elaphus) which possessed antibodies to type C aphthovirus. This finding was not confirmed by subsequent investigations of deer of the same species, in which 77 samples were taken for virus isolation.

No case of F M D was found in other members of the same deer populat ion, nor in domestic animals in the same area. The significance of such seroconversions thus remains to be shown.

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T A B L E I V

Principal African species receptive to the virus of foot and mouth disease

(according to 49)

Order/Family Common name Scientific name

Artiodactyla Bovidae Eland

Bushbuck Greater kudu African buffalo Common duiker Waterbuck Reedbuck Roan antelope Sable antelope Gemsbok Tsessebe Red hartebeest Brindled gnu Cape grysbok Thomson's gazelle Impala

Taurotragus spp. Tragelaphus scrip tus Tragelaphus strepsiceros Syncerus caffer Sylvicapra grimmia Kobus ellipsiprymnus Redunca arundinum Hippotragus equinus Hippotragus niger Oryx gazella Damaliscus lunatus Alcelaphus buselaphus Connochaetes taurinus Raphicerus melanotis Gazella thomsoni Aepyceros melampus

Cervidae Fallow deer Dama dama Giraffidae Giraffe Giraffa camelopardalis Suidae Bush pig

Warthog Potamochoerus porcus Phacochoerus aethiopicus

Camelidae Dromedary Camelus dromedarius

Insectívora Erinaceidae African hedgehog Atelerix albiventris

Rodentia Muridae African rat Arvicanthis abyssinicus Rhizomyidae Mole rats Terchyoryctes spp. Hystricidae Porcupines Hystrix galeata

Proboscidea Elephantidae African elephant Loxodonta africana

In Switzerland wild boar became infected during an outbreak in 1960, while in the USSR the saiga (Saiga tatarica) has been incriminated.

African horse sickness

This disease seems to have originated on the African continent, but did not become recognised until susceptible animals were introduced from Europe into South Africa. Only since then is there evidence of a primary reservoir among wild species.

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Most of the zebras in South Africa possess specific ant ibody. Experimental infection of zebras (35) results in a mild disease with a febrile attack, and occasionally oedematous swelling of the hollow above the eyes. Viraemia lasts for 18 days. The viraemic period may be important in the transmission of the virus by ar thropod vectors.

The disease has made brief incursions into Europe , particularly Spain (28, 121) where the vector insects occur (72). The last incursion in 1987 probably resulted from the introduction of zebras from Namibia.

Pestiviral infections

The recently defined pestivirus group comprises viruses of Artiodactyla having close antigenic relationships (83). The three main pestiviruses isolated so far are classical swine fever virus, bovine diarrhoea pestivirus ( B V D / M D virus) and border disease virus of sheep. These viruses are pathogenic for their respective natural hosts, and are capable of infecting other species (cross-infection). They possess the important property of being able to cross the placenta, producing congenital infection (150).

A disease resembling mucosal disease (MD) of cattle has been described in free-living deer and among ruminants in a zoo, but without laboratory confirmation. Similarly, cases of classical swine fever have been reported in wild boar , notably in breeding premises for repopulation, and serological reactions to classical swine fever virus have been demonstrated in wild boar (15).

Pestiviruses have been isolated from roe deer (Capreolus capreolus) (122), red deer (Cervus elaphus) (80) and fallow deer (Dama dama) (152) found dead, but the contribution of virus to the disease is uncertain. Pestiviruses have also been obtained from African buffalo (Syncerus caffer), giraffe (Giraffa camelopardalis) and gnu (Connochaetes spp.) (131).

Experimental infection of red deer (Cervus elaphus) results in serological conversion (70).

Serological surveys have shown that numerous species of ruminants in Europe , North America and Africa (131) possess antibodies to BVD virus, but at low incidence (64, 40, 60, 31). Thus a recent serological survey of red deer (Cervus elaphus) in the United Kingdom revealed an incidence of only 5 % (Nettleton et al., unpublished results), and the situation is similar in France (15).

The role of the wild fauna in the epidemiology of pestiviral infections remains to be elucidated. In the present state of knowledge, wild species do not seem to play a determinant role in transmitt ing infection to domestic cattle. Here infection is acquired essentially from immunotolerant cattle with persistent viraemia (81, 92).

C O N C L U S I O N S A N D R E C O M M E N D A T I O N S

In order to establish the potential role of the wild fauna in the persistence and dissemination of an infection shared with domestic animals, it is necessary to answer the questions posed by Anderson (5) in connection with foot and mouth disease:

a) Which species are susceptible to infection?

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b) Do these species develop clinical disease and do they excrete the causal agent accordingly?

c) Which species become asymptomatic carriers after infection? d) Are the wildlife carriers capable of transmitting the disease to other animals,

particularly domestic species ?

On the basis of these criteria, the diseases can be arranged roughly in three categories:

1. Diseases having a known wildlife reservoir, such as rabies, African swine fever and malignant catarrhal fever.

2. Diseases affecting many domestic a n d / o r wild species but without a known wildlife reservoir, such as rinderpest.

3. Diseases distributed equally between wild and domestic animals.

In the light of present information, it is often necessary to reconsider our att i tude towards wildlife, which has been wrongly accused in the past of being the source of most of the epizootic diseases affecting domestic animals.

On the contrary, the history of rinderpest has shown that it may be necessary to prevent contact between domestic and wild animals in order to protect the latter.

If wild animals are to be regarded as sources of protein and potential for recreation, the problem must be viewed from two aspects: not only the risk incurred by domestic animals in contact with wild animals, but also the risk incurred by wild animals in contact with domestic animals. In addition, action may become necessary to improve the health of the wild species, particularly in ecologically disturbed zones.

It must always be remembered that many infections and infestations are strictly specific and are not shared. The actual significance of the results of laboratory tests often needs to be re-examined.

One reason why epidemiological interactions between wild and domestic animals have been little understood in the past is that studies have been made from the medical perspective alone, ignoring the ecological factors which govern pathological manifestations (128).

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The economic and cultural status of wild species has undergone considerable change in recent years.

In order to derive the most benefit from the economic and cultural development of wildlife, it is vital to improve our knowledge of the pathological aspects neglected until now. Our knowledge is often fragmentary or inadequate. It should be set in the context of a more or less stable ecological system in which human beings also participate.

A scheme for organising veterinary research for the rational use of wildlife was proposed by Croze in 1981 (26). Application of such a scheme implies a readjustment of thinking and a transformation of certain objectives currently pursued in veterinary research.

Certain scientists, however, seem to assume that the disease factor can be neglected among wild species. This att i tude is not justified by our existing knowledge (43).

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Modification of natural ecological systems by bringing animals together in farms leads to the appearance of new diseases, and upsets the host-parasite relationship.

In addition, there is often little or no information about the infections and infestations of the wild fauna. Research needs to be conducted on many subjects, including the specific infections of wildlife. Existing evidence of the intervention of pathogens of domestic animals in wildlife is often indirect (serological evidence). Each case requires verification by experimental inoculation to discover if species reputed to be susceptible really are so.

Diagnostic tests need improved specificity, and they may have to be adapted to meet the actual situation. Our epidemiological tools are, in fact, often unsuitable.

A C K N O W L E D G E M E N T S

The authors are grateful to Marinette Muys for preparing the typescript and to Mr Amaury Breuls de Tiecken for assistance in identifying the names of species. They also wish to acknowledge assistance received from Dr L. Blajan, Director General of the OIE , Georges Mees, Alex Donaldson and Fiona Stuart . Useful criticism of the manuscript was provided by Walter Plowright, Claude Louzis and Y. Ozawa. Thanks are also extended to the translators.

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REFERENCES

(see p. 696)

diseases of wild animals transmissible to domestic animals

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