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Prevalence and Clinical Significance of Herpesvirus Infection in Populations of Australian Marsupials

Kathryn Stalder - Affiliations The Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Melbourne, Victoria, Australia, Australian Wildlife Health Centre, Healesville Sanctuary, Healesville, Victoria, Australia

Paola K. Vaz - Affiliation: The Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Melbourne, Victoria, Australia

James R. Gilkerson - Affiliation: The Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Melbourne, Victoria, Australia

Rupert Baker - Affiliation: Australian Wildlife Health Centre, Healesville Sanctuary, Healesville, Victoria, Australia

Pam Whiteley - Affiliation: The Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Melbourne, Victoria, Australia

Nino Ficorilli - Affiliation: The Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Melbourne, Victoria, Australia

Liliana Tatarczuch - Affiliation: The Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Melbourne, Victoria, Australia

Timothy Portas - Affiliation: Veterinary and Research Centre, Tidbinbilla Nature Reserve, Via Tharwa, Australian Capital Territory, Australia

Kim Skogvold - Affiliations Conservation Medicine Program, School of Veterinary and Life Sciences, Murdoch University, Perth, Western Australia, Australia, Perth Zoo Veterinary Department, Perth Zoo, South Perth, Western Australia, Australia

Garry A. Anderson - Affiliation: The Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Melbourne, Victoria, Australia

Joanne M. Devlin - Affiliation: The Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Melbourne, Victoria, Australia 


ABSTRACT

Herpesviruses are enveloped, double stranded DNA viruses that have been identified in species across the animal kingdom, including vertebrate and invertebrate species. Extensive coevolution of herpesviruses with their host species is thought to be largely responsible for their exceptional adaptation to their natural hosts, and plays an important role in their survival strategy [1,2]. Herpesviruses are well known for their capacity to induce lifelong infections. Herpesvirus infections are characterised by a primary infection event, with or without acute disease, followed by variable periods of subclinical latency, with subsequent episodes of virus reactivation and shedding during periods of stress or immune-compromise. It is this biological strategy that contributes significantly to the survival and dissemination success of herpesviruses in their host species [2]. Herpesviruses were first identified in Australian marsupials in 1975 when an outbreak of disease and sudden death in a group of captive parma wallabies (Macropus parma) led to the isolation of what is now known as Macropodid herpesvirus 1 (MaHV-1) from the renal tissue of an affected animal [3]. Affected wallabies exhibited various clinical and pathological abnormalities; including rhinitis, conjunctivitis, pneumonia, cloacal ulceration, and variable splenic, pulmonic and hepatic necrosis. Intranuclear inclusion bodies were occasionally identified [3]. Since then, further outbreaks of disease in various macropod species have led to the discovery of three additional herpesvirus species. Macropodid herpesvirus 2 (MaHV-2), an alphaherpesvirus similar but distinct from MaHV-1 [4,5] was detected in samples from grey dorcopsis wallabies (Dorcopsis luctuosa) and a quokka (Setonix brachyurus). Macropodid herpesvirus 3 (MaHV-3), a gammaherpesvirus, was identified in captive and free-living eastern grey kangaroos (Macropus giganteus) [6,7]; and recently Macropodid herpesvirus 4 (MaHV-4), an alphaherpesvirus associated with respiratory and possibly neurological disease was detected in a free-living eastern grey kangaroo [8]. A wide range of Australian marsupials (up to 23%) were found to have virus neutralising antibodies against MaHV-1 in an early seroprevalence study, with higher prevalence and antibody titres found to be associated with captivity and advancing age [9]. More recently a gammaherpesvirus, denoted Potoroid herpesvirus 1 (PotHV-1), was identified in four free-living eastern bettongs (Bettongia gaimardi) as part of a comprehensive health surveillance program during translocation [10]. Two gammaherpesviruses have also been recently identified in koalas (Phascolarctos cinereus) [11,12] and a novel gammaherpesvirus species was found in a yellow-footed antechinus (Antechinus flavipes) and an agile antechinus (Antechinus agilis) [13]. Whilst herpesvirus particles have been detected by electron microscopy in a common wombat (Vombatus ursinus) [14], molecular detection and classification of wombat herpesviruses have not previously been reported. Many Australian marsupial species are now considered vulnerable and threats to the survival of populations include habitat destruction through urbanisation or fire, introduced predators and competitors, inbreeding and disease. These threats have been better characterised for some species than others, and the risk and consequences of herpesvirus infections in these populations remains to be quantified. Whilst most herpesvirus outbreaks reported in Australian marsupials have occurred within captive environments [3,15–17], the identification of MaHV-3 in a group of free-ranging eastern grey kangaroos exhibiting respiratory disease [7] and the isolation of MaHV-4 from a free-living eastern grey kangaroos with respiratory disease [8], indicates that some herpesviruses may have the potential to negatively impact free-living marsupial populations. This study aimed to examine the prevalence of herpesviruses in samples collected from captive and free-ranging Australian marsupials using molecular and serological techniques. This study also aimed to identify any risk factors or signs of disease associated with herpesvirus infection in these animals. The marsupial populations targeted included koalas, eastern grey kangaroos (Macropus giganteus) and common wombats. Samples from other marsupial species were also included opportunistically.