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Rev. sci. tech. Off. int. Epiz., 1988, 7 (4), 977-988. Herpesvirus infections in Cervidae P.F. NETTLETON *, E. THIRY **, H. REID * and P.-P. PASTORET ** Summary: The earliest evidence of herpesvirus infections of Cervidae came from testing free-living deer for antibody to bovine herpesviruses pathogenic to cattle. Antibody to the cattle alphaherpesvirus bovine herpesvirus type 1 (BHV-1), the causative agent of infectious bovine rhinotracheitis (IBR), has been demonstrated in mule deer, white-tailed deer and caribou in North America and in red deer, roe deer, reindeer and fallow deer in Europe. Alphaherpesviruses serologically related to BHV-1 have been isolated from red deer and reindeer. The red deer virus, herpesvirus of Cervidae type 1 (HVC-1), was recovered from farmed red deer calves with ocular disease. The reindeer virus was isolated from an animal which had been treated with dexamethasone and no disease attributable to a herpesvirus has been seen in this species. Biochemical and serological studies have demonstrated that these two viruses are distinct from each other and from BHV-1. Experimental infections of cattle with the two viruses have induced no or mild disease. The one serious disease recognised in Cervidae due to herpesvirus infection is malignant catarrhal fever (MCF). The wildebeest-associated gammaherpesvirus, alcelaphine herpesvirus-1 (AHV-1), has caused deaths of white-tailed deer, sika deer, barasingha deer and reindeer among captive populations in zoological parks, while MCF due to the sheep-associated agent, believed to be a gammaherpesvirus, is common among several species of farmed deer and represents a serious threat to these new domestic livestock. Deer do not shed infectivity, thus the disease does not spread from affected animals. The disease has not been reported to affect free-living animals. KEYWORDS: Cattle diseases - Cervidae - Farmed deer - Herpesvirus infections - Malignant catarrhal fever virus - Serological techniques - Wild animals. INTRODUCTION Several species of free-living deer have the opportunity for frequent contact with cattle, sheep and goats, and have long been viewed with suspicion as potential sources of infection for at least these three domestic ruminants. As early as 1964, only eight years after being confirmed as the cause of infectious bovine rhinotracheitis in cattle, bovine herpesvirus type 1 (BHV-1) was shown to be capable of infecting mule deer (Odocoileus hemionus) experimentally (2). Since then, serological surveys of free- * Moredun Research Institute, 408 Gilmerton Road, Edinburgh, United Kingdom. ** Department of Virology-Immunology, Faculty of Veterinary Medicine, University of Liège, 45, rue des Vétérinaires, 1070 Brussels, Belgium. 978 living deer populations for antibody to BHV-1 and other herpesviruses have revealed further evidence of infections. The direct contact normally required for the natural transmission of herpesviruses is however unlikely to occur between different species of free-living deer and between free-living deer and domestic livestock. The early serological findings are now best explained by the good evidence that free-living red deer (Cervus elaphus) and reindeer (Rangifer tarandus) are infected with their own distinct herpesviruses which are serologically related to each other and t o BHV-1 (7, 8, 10, 15, 35). N o disease due to a herpesvirus has ever been confirmed in free-living deer and there is n o evidence that they may act as reservoir hosts for any herpesvirus of other domestic livestock. The importance of herpesvirus infections of deer has become apparent only as these species have been developed as domestic livestock and kept in zoological collections. Herpesviruses, serologically related to B H V - 1 , have been isolated from farmed red deer and domesticated reindeer and malignant catarrhal fever, either confirmed or believed to be due to a herpesvirus infection, has resulted in serious losses among farmed and zoo deer. The three sections in this paper will cover: evidence of herpesvirus infections of deer from serological surveys, a comparison of the herpesviruses of red deer and reindeer with those from other domestic livestock and, malignant catarrhal fever. SEROLOGICAL EVIDENCE OF HERPESVIRUS INFECTIONS OF C E R V I D A E Herpesviruses are among the most successful of all virus groups and have been demonstrated in virtually every species of vertebrate that has been investigated. A subdivision of the herpesvirus family into three major sub-groupings, alpha-, betaand gammaherpesviruses, is possible on the basis of differences in biological properties. T h e alphaherpesviruses comprise the rapidly growing cytolytic viruses which establish latent infections primarily in neural tissue; the betaherpesviruses comprise the cytomegaloviruses which grow slowly in culture and can establish latent infection in several tissue sites; and the slow-growing gammaherpesviruses, which are lymphotropic (33). Alphaherpesviruses Virtually all the early serological testing of deer was with the cattle alphaherpesvirus, B H V - 1 ; six species of deer were shown to be infected. Since the recovery of deer alphaherpesviruses, more extensive surveys using these agents have added to the knowledge of their prevalence among deer (Table I). There is thus evidence of infection in four species of deer in E u r o p e and two in N o r t h America with red deer, reindeer and mule deer showing high levels of infection. Given the evidence of antibody to BHV-1 in sera from twenty species of free-living African ruminants, feral water buffalo (Bubalus bubalis) in Australia and pronghorn antelope (Antilocapra americana) in North America (27, 39), it is likely that many ruminants are infected with related alphaherpesviruses and that future investigations in other species of deer will reveal positive findings. The relationship between such viruses is explored below. 979 TABLE I Species of deer with serological evidence of infection with a virus antigenically related to bovine herpesvirus 1 Species Red deer (Cervus elaphus) Country % positive References 50 520 70 16 29 11 (19) (24) (40) 80 1 (40) 13 13 18 39 (17) (18) BHV-1 BHV-1 85 172 553 30 France German Dem. Rep. German Dem. Rep. Italy USA BHV-1 BHV-1 BHV-1 BHV-1 387 71 1,305 83 BHV-1 BHV-1 43 50 2 36 (13) (2) USA BHV-1 198 2 (12) Scotland Britain Belgium France Reindeer (Rangifer tarandus) Roe deer (Capreolus capreolus) Fallow deer (Dama dama) Mule deer (Odocoileus hemionus) White-tailed deer (Odocoileus virginianus) German Dem. Rep. Finland Canada Test viruses No. tested BHV-1 HVC-1 BHV-1 HVC-1 BHV-1 HVC-1 BHV-1 0.8 1 3 3 (8) (9) (40) (17) (18) (18) There is little information on serological testing with other alphaherpesviruses. Although antibody to bovine herpesvirus type 2 (BHV-2) (bovine herpes mammillitis virus) has been demonstrated in seventeen species of African wild ruminants (21), evidence of the infection in deer is p o o r . Less than 1% of 387 sera from roe deer (Capreolus capreolus) in France were positive. Eighty sera from Belgian roe deer were all negative, as were 150 sera from red deer in these two countries (40). Aujeszky's disease virus (Pseudorabies virus) has caused natural infections of roe deer in Eastern E u r o p e ; this virus, which is an alphaherpesvirus of swine capable of causing serious disease in a wide range of secondary hosts, has been shown experimentally to infect white-tailed deer (Odocoileus virginianus) (43). Infection of secondary hosts with equid herpesvirus 1 (EHV-1), the agent of equine rhinopneumonitis, has also been demonstrated. The virus has been isolated from fallow deer (Dama dama) (16, 41) and from antelope (3, 21). Betaherpesviruses There is no evidence of betaherpesvirus infections of deer. Four hundred and sixtyseven roe deer and 150 red deer sera collected in France and Belgium were all negative for antibody to bovine herpesvirus 4 (BHV-4) (40). 980 Gammaherpesviruses There are no reports of antibody to gammaherpesviruses in deer. Known gammaherpesvirus infections of deer are usually fatal (see "malignant catarrhal fever" below). Serological cross-relationships have been reported between B H V - 1 , BHV-4 and alcelaphine herpesvirus 1 (AHV-1), the cause of wildebeest-derived M C F (6, 36, 37). These relationships are only partial but should be taken into account in serological surveys of wild ruminants, since they may give rise to doubtful positive reactions. COMPARISON OF ALPHAHERPESVIRUSES FROM RED DEER A N D REINDEER WITH THOSE FROM OTHER SPECIES In 1982, an alphaherpesvirus serologically related to BHV-1 was isolated from pooled ocular/nasal swabs from farmed red deer calves suffering from eye disease (15). T h e same virus was recovered from further outbreaks of eye disease in farmed red deer calves in 1983 (24) and clinical disease similar to that caused by the virus has been seen since in market-purchased red deer calves in Scotland. The red deer herpesvirus has been tentatively designated herpesvirus of Cervidae type 1 (HVC-1) (32). Red deer newly imported into Denmark have also yielded an alphaherpesvirus following glucocorticoid treatment (35). A n alphaherpesvirus was recently isolated from the vagina of a reindeer treated experimentally with dexamethasone (7), but n o disease attributable to infection has ever been observed. This herpesvirus has been tentatively designated herpesvirus of Cervidae type 2 (HVC-2) (22). Serological comparison Both HVC-1 and HVC-2 are serologically related to BHV-1. Cross-neutralisation results between HVC-1 and BHV-1 using hyperimmune rabbit sera and convalescent red deer and cattle sera reveal significant differences between the viruses (Table II). A similar relationship between H V C - 2 and BHV-1 is suggested by the one-way neutralisation of the two viruses by antisera against BHV-1 (7). TABLE Serological relationship II between HVC-1 and BHV-1 Virus Antisera HVC-1 BHV-1 Anti HVC-1 Rabbit Red deer 2.17* 4.13 0.49 1.38 Anti BHV-1 Rabbit Bovine 3.47 4.36 3.65 6.03 * Results expressed as log5 assay 10 neutralisation index based on a plaque reduction 981 FIG. 1 Red deer calf suffering from severe ocular disease associated with H V C - 1 infection Both eyes are closed, there is copious mucopurulent discharge from the right eye and supraorbital oedema is prominent over both eyes (Photograph courtesy of Dr D . M . Inglis) A recent serological comparison has been m a d e between B H V - 1 , HVC-1 and bovine herpesvirus 6 (BHV-6) (also k n o w n as caprine herpesvirus 1), an alphaherpesvirus of goats which has a serological one-way cross reactivity with BHV-1 (25). Both neutralisation and E L I S A tests were capable of distinguishing readily between serological reaction to the three viruses when quantitative comparisons were made. The results suggested that HVC-1 and BHV-6 are more closely related to BHV-1 t h a n they are t o each other. In c o m m o n with previous reports (15, 35), convalescent sera from red deer had neutralising antibody titres two to sixteen-fold higher to HVC-1 than to B H V - 1 . The significance of these findings has implications for the diagnosis and control of alphaherpesvirus infections of ruminants. At the present time, the international movement of such livestock often requires serological testing for the absence of antibody to B H V - 1 . Clearly, in the light of present knowledge, only cattle should undergo such tests. If it is desired to control the spread of HVC-1 in red deer, HVC-2 in reindeer or BHV-6 in goats, serological testing with the homologous virus would be more sensitive and should be adopted. The use of monoclonal antibodies (Mabs) will be helpful in elucidating the relationships a m o n g ruminant herpesviruses. Preliminary results with a panel of 11 Mabs raised against BHV-1 (strain 6660) (23) have shown that 6 detected all of 982 18 BHV-1 isolates in an indirect immunofluorescence test, while the other 5 detected at least 15 of these isolates. Only 2 of the Mabs reacted with HVC-1 under the same conditions, emphasising further the antigenic distinction of this virus from BHV-1 ( P . F . Nettleton, unpublished data). Biochemical characterisation N o detailed study of the biochemistry of the deer alphaherpesviruses has yet been carried out. Restriction endonuclease analysis of viral D N A has shown that HVC-1 a n d H V C - 2 have D N A distinct from each other and from BHV-1 ( A . J . Herring, personal communication; 35). The significance of this finding gives n o clue to the true relationship between the genomes of the deer viruses and B H V - 1 . It is k n o w n that BHV-6 and BHV-1 share a high degree of base sequence homology even t h o u g h they have significantly different restriction site maps (11). A greater knowledge of the molecular biology of the deer herpesviruses will m a k e a useful contribution to our understanding of the evolution and current relationships between ruminant alphaherpesviruses. Pathogenicity for deer and cattle The experimental intranasal infection of two red deer with HVC-1 resulted in mild clinical disease of rhinitis and conjunctivitis; virus was recovered from nasal and ocular swabs from both deer for u p to seven days post-infection. In contrast, two bovine calves receiving the same virus showed no clinical disease, and virus was only recovered from nasal swabs from one of the calves for two days post-infection. When challenged with BHV-1 eighty-four days after the infection with H V C - 1 , both calves developed pyrexia and nasal discharges and virus was recovered in nasal and ocular swabs for seven days after infection (32). This lack of susceptibility of cattle to HVC-1 has been further confirmed. Following intranasal instillation of a Danish isolate of HVC-1 into two heifers, virus could only be reisolated from one animal one day after challenge and not during the following eleven days (35). The susceptibility of cattle to H V C - 2 may be greater. Mild symptoms of rhinitis without any evidence of systemic disease have been reported, with virus being reisolated for six to nine days after infection (22). Two species of deer have been experimentally infected with B H V - 1 . Six mule deer were susceptible; anorexia, depression and respiratory disease occurred two t o four days after infection, and virus was recoverable from nasal swabs for five days after inoculation. The pattern of antibody response was similar to that of cattle (2). T w o red deer were not susceptible; no disease occurred, virus was recovered from only one of the deer for two days post-infection and there was no evidence of seroconversion (32). At the present time, it seems evident that alphaherpesviruses from deer, as well as those from buffalo and goats (1), occur only in their natural hosts and do not cross stably into other species. 983 M A L I G N A N T C A T A R R H A L FEVER Malignant catarrhal fever is a fatal disease of cattle, deer and some other ruminants, which is characterised by a p a t h o g n o m o n i c pathology of widespread cell necrosis and lymphoid cell proliferation. The clinical disease in deer is usually rapid, with affected deer separating from the group, being lethargic and anorexic and having diarrhoea or dysentery. T h e disease can result in " s u d d e n - d e a t h " but if the animal survives for u p to a week, other clinical signs include ocular and nasal discharges, erosions o n the oral mucosa, corneal opacity, enlarged surface lymph nodes, excitability a n d muscle t r e m o r s , a n d patchy exanthema with ulceration in the perineum. At necropsy, cardinal features are multiple raised white spots 1-2 m m in diameter o n the kidneys, erosions of buccal papillae and haemorrhagic areas on the epithelial surfaces of the a b o m a s u m and urinary bladder. Although M C F is recognised as a single clinico-pathological entity it has at least two causes. In Africa, the cause is well-established and provides a classic example of how a gammaherpesvirus (AHV-1), which is prevalent a n d apparently innocuous in its natural host the wildebeest (Connochaetes taurinus), causes severe disease when it infects other species. Under natural conditions, losses occur in cattle grazing pasture to which wildebeest calves also have access, but in zoological parks AHV-1 has spread from wildebeest to cause deaths in white-tailed deer (44, 45), sika deer (Cervus nippon) (38), barasingha deer (Cervus duvauceli) (14) and possibly also elk (Alces alces) and reindeer (Altmann, cited in 27) and Père David's deer (Elaphurus davidianus) (42). Outside Africa, the cause of M C F remains u n k n o w n , although there is strong circumstantial evidence t h a t sheep are the source of infection and there is growing evidence to support the hypothesis that a sheep gammaherpesvirus, serologically related to A H V - 1 , causes "sheep-associated" M C F . This form of M C F occurs worldwide wherever sheep are in contact with cattle and farmed deer. Losses in cattle are sporadic, generally involving few animals, but deer appear much more susceptible and extensive outbreaks have occurred in farmed red deer (20, 30, 34), axis deer (Axis axis) (4), rusa deer (Cervus timorensis) (5) and Père David's deer (31) as well as in mule deer (26). In contrast to the disease in cattle, it has proved relatively easy t o transmit the disease from deer to other deer a n d rabbits a n d this has contributed substantially to knowledge o n the pathogenesis of the disease (29). T h e latest hypothesis proposes that the gammaherpesvirus preferentially infects a specific subset of lymphoid cells, which dysfunction to give rise to an interleukin driven polyclonal T-lymphocyte hyperplasia and dysfunction of natural killer activity, resulting in widespread a u t o i m m u n e destruction of normal tissues. This hypothesis is consistent with the lack of demonstrable virus and the principal features of the pathological process, namely: widespread cell necrosis and lymphoid cell proliferation. There is serological evidence that several species of African antelope as well as members of the subfamily Caprinae are infected with an antigenically related gammaherpesvirus and m a y also constitute reservoirs of M C F infection for deer and cattle (28). While M C F is a serious disease of farmed deer, there is n o evidence that deer can transmit the disease to other species. Like cattle, they appear to be a dead-end or indicator host for gammaherpesviruses from other species. 984 CONCLUSIONS The herpesviruses of free-living deer have so far posed n o threat to other domestic livestock. The domestication of deer has led to the recognition of ocular disease in farmed red deer due to HVC-1 and to the demonstration of the marked susceptibility of several species of deer to M C F . The isolation and further characterisation of new and existing cervid herpesviruses is essential to our understanding of the likely role of these agents in farmed deer and will give greater insight into the evolution and current relationships between ruminant herpesviruses. * * * LES INFECTIONS HERPÉTIQUES DES CERVIDÉS. - P.F. Nettleton, E. Thiry, H. Reid et P.-P. Pastoret. Résumé : Les premières preuves de l'existence d'infections herpétiques chez les cervidés ont été obtenues en recherchant, chez ces animaux vivant en liberté, des anticorps vis-à-vis des herpèsvirus pathogènes pour les bovins. Des anticorps vis-à-vis de l'herpèsvirus bovin de type 1 (BHV-1, alphaherpèsvirus bovin), agent de la rhinotrachéite infectieuse bovine (IBR), ont été mis en évidence, en Amérique du Nord, chez le cerf-mulet, le cerf de Virginie et le caribou et, en Europe, chez le cerf rouge, le chevreuil, le renne et le daim. Des alphaherpèsvirus sérologiquement apparentés au BHV-1 ont été isolés chez les cerfs rouges et les rennes. Le virus du cerf, herpèsvirus des cervidés de type 1 (HVC-1), a été isolé chez des jeunes cerfs d'élevage atteints d'une maladie oculaire. Le virus du renne a été isolé d'un animal qui avait été traité à la dexaméthasone ; aucune maladie pouvant être imputée à un herpèsvirus n 'a été observée chez cette espèce. Les études biochimiques et sérologiques ont prouvé que ces deux virus sont distincts l'un de l'autre et du BHV-1. L'infection expérimentale de bovins par ces deux virus n'a eu que peu ou pas d'effet pathologique. La seule maladie grave reconnue chez les cervidés qui soit due à un herpèsvirus est le coryza gangréneux. Le virus des alcélaphinés de type 1 (AHV-1), gammaherpèsvirus associé au gnou, a provoqué des mortalités chez des cerfs de Virginie, des cerfs sika, des barasinghas et des rennes en captivité dans des jardins zoologiques, tandis que le coryza gangréneux associé au mouton, dont on présume que l'agent est un gammaherpèsvirus, est fréquent chez plusieurs espèces de cerfs d'élevage et représente une menace sérieuse pour ces animaux nouvellement domestiqués. Les cerfs n'excrètent pas l'agent infectieux ; la maladie n'est donc pas propagée par les animaux atteints. Elle n'a pas été signalée chez les animaux vivant en liberté. MOTS-CLÉS : Animaux sauvages - Cerfs d'élevage - Cervidés - Infections herpétiques - Maladies des bovins - Techniques sérologiques - Virus du coryza gangréneux. * * * 985 INFECCIONES POR HERPESVIRUS EN LOS CÉRVIDOS. - P.F. Nettleton, E. Thiry, H. Reid y P.-P. Pastoret. Resumen: Las primeras pruebas de la existencia de infecciones herpéticas en los cérvidos se obtuvieron al buscar en estos animales, que vivían en libertad, anticuerpos a los herpesvirus patógenos para los bovinos. En Norteamérica, se descubrieron anticuerpos al herpesvirus bovino de tipo 1 (BHV-1, alfaherpesvirus bovino), agente de la rinotraqueitis infecciosa bovina (IBR), en el ciervo mula, el ciervo de Virginia y el caribú y, en Europa, en el ciervo rojo, el corzo, el reno y el gamo. En los ciervos rojos y en los renos, se aislaron alfaherpesvirus serológicamente emparentados con el BHV-1, mientras que el virus del ciervo, herpesvirus de los cérvidos de tipo 1 (HVC-1), se aisló en animales jóvenes de cría afectados por una enfermedad ocular. El virus del reno se aisló en un animal que había sido tratado con dexametasona, pero no se observó ninguna enfermedad que pudiera atribuirse a un herpesvirus en esta especie. Los estudios bioquímicos y serológicos demostraron que estos dos virus son distintos no sólo no de otro, sino también del BHV-1. La infección experimental de bovinos por estos dos virus no tuvo ningún efecto patológico o casi ninguno. La única enfermedad grave reconocida en los cérvidos que se debe a un herpesvirus es la fiebre catarral maligna. El virus de los alcelafinos de tipo 1 (AHV-1), gammaherpesvirus relacionado con el ñu, provocó casos mortales en ciervos de Virginia, ciervos sika, barasinghas y renos cautivos en jardines zoológicos, mientras que la enfermedad relacionada con el carnero, cuyo agente se presume que es un gammaherpesvirus, es frecuente en varias especies de ciervos de cría y representa una seria amenaza para estos animales recientemente domesticados. Los ciervos no excretan el agente infeccioso, es decir que la enfermedad no es propagada por los animales afectados. No se ha señalado la presencia de ésta en los animales que viven en libertad. 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