D8387.PDF

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.
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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.
PALABRAS CLAVE: Animales salvajes - Cérvidos - Ciervos de cría Enfermedades de bovinos - Infecciones herpéticas - Técnicas serológicas - Virus
de la fiebre catarral maligna.
*
* *
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