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Lucy Woolford BSc BVMS (Hons) PhD MACVSc

Doctor of Philosophy Thesis

Papillomatosis and Carcinomatosis in the Western Barred Bandicoot (Perameles bougainville)

Supervisors

  • Dr Amanda O’Hara BSc (Hons), BVMS MACVSc DACVP Murdoch University
  • Dr Phillip Nichols BSc(Hons) BVSc PhD MRCVS MRCPath, Murdoch University
  • Dr Kris Warren BSc BVMS (Hons) PhD, Murdoch University

Conservation efforts to prevent the extinction of the endangered western barred bandicoot Perameles bougainville (WBB) are currently hindered by a debilitating skin disease, characterised by progressive papillomas (warts), carcinoma in situ and squamous cell carcinomas. Now extinct on mainland Australia, wild populations of the WBB are known only to exist on Bernier and Dorre Islands in Shark Bay, Western Australia.

Research performed by Dr Woolford and her colleagues describes and analyses the features of this skin disease (including microscopic and ultrastructural features of skin cancers). It also describes the discovery and characterisation of a novel virus associated with this disease, the bandicoot papillomatosis carcinomatosis virus type 1 (BPCV1). Using molecular (DNA-based) and immunohistochemical techniques, BPCV1 was identified within cutaneous and muco-cutaneous papillomas and carcinomas. Sequencing of the virus genome as part of this research yielded very interesting and unique findings: the genomic structure and encoded genes of BPCV1 are similar to two different virus families: the Papillomaviruses and Polyomaviruses. BPCV1 is the first reported virus which essentially appears to be ‘hybrid’ of two very well characterised virus families. BPCV1 has been proposed as the first member of a new family of viruses, and a similar virus has since been discovered in another bandicoot species. These unique bandicoot viruses provides further insight into the evolution of the ancient DNA virus families, Papillomaviridae and Polyomaviridae, which play important roles in both cancer and non-neoplastic disease in humans and many animal species.

Epidemiological studies were also performed, examining the prevalence and distribution of both this disease and the virus in wild, captive and re-introduced populations of WBBs in Western Australia. BPCV1 and the disease were found in the wild WBB population at Red Cliff on Bernier Island, and in mainland populations established from all or a proportion of founder WBBs from Red Cliff. BPCV1 and the disease were not found in the wild population on Dorre Island, or in the mainland population founded by animals exclusively from Dorre Island. WBB populations on Bernier and Dorre Islands have been separated from one another for over 3000 years, and some genetic variation exists between the two populations. However, no difference in susceptibility to the disease was found between Dorre Island, Bernier Island and island-cross individuals. Increasing age was found to be the most significant risk factor for development of this disease. Epidemiological findings from this study support the pathological and molecular association between BPCV1 infection and the papillomatosis and carcinomatosis syndrome.

Further studies will hopefully increase our understanding of this disease, the virus that has been implicated in its pathogenesis, and the interaction between the bandicoot immune system and viral infection. The papillomatosis and carcinomatosis syndrome in the western barred bandicoot is a pertinent example of a disease process hampering efforts to prevent the extinction of an endangered species.

This thesis is available in Murdoch University's Digital Thesis collection - http://wwwlib.murdoch.edu.au/adt/

Publications

  • Woolford L, Bennett MD, Sims C, Thomas N, Friend JA, Nicholls PK, Warren KS & O’Hara AJ (2009) Prevalence, emergence and factors associated with a viral papillomatosis and carcinomatosis syndrome in wild, reintroduced and captive western barred bandicoots (Perameles bougainville). EcoHealth. Epub ahead of print 7 November 2009.
  • Woolford L, O'Hara AJ, Bennett MD, Slaven M, Swan RA, Friend JA, Ducki A, Sims C, Hill S, Nicholls PK & Warren KS (2008) Cutaneous papillomatosis and carcinomatosis in the western barred bandicoot (Perameles bougainville). Veterinary Pathology. 45(1): 95-103.
  • Woolford L, Rector A, Van Ranst M, Ducki A, Bennett MD, Nicholls PK, Warren KS, Swan RA, Wilcox GE & O’Hara AJ (2007) A novel virus detected in papillomas and carcinomas of the endangered western barred bandicoot (Perameles bougainville) exhibits genomic features of both the Papillomaviridae and Polyomaviridae. Journal of Virology 81(24): 13280-13290 [Featured on 81(24) journal cover and ‘Spotlight’ for noteworthy articles].
  • Bennett MD, Woolford L, Stevens H, O’Hara AJ, Warren KS and Nicholls PK (2008) Genomic characterization of a novel virus found in papillomatous lesions from a southern brown bandicoot (Isoodon obesulus) in Western Australia. Virology 376(1): 173-82.
  • Bennett, MD, Woolford L, O'Hara AJ, Warren KS and Nicholls PK (2008) In situ hybridization to detect bandicoot papillomatosis carcinomatosis virus type 1 in biopsies from endangered western barred bandicoots (Perameles bougainville). Journal of General Virology 89(2): 419-23.
  • Bennett M D, Woolford L, O'Hara AJ, Nicholls PK and Warren KS (2008) Clinical chemistry and tissue enzyme activities in western barred bandicoots (Perameles bougainville). Veterinary Clinical Pathology 37(2): 221-4.
  • Bennett MD, Woolford L, Nicholls PK, Warren KS, and O'Hara AJ (2008) Hepatic intranuclear glycogen inclusions in western barred bandicoots (Perameles bougainville), Journal of Veterinary Diagnostic Investigation 20: 376-379.
  • Bennett MD, Woolford L, O'Hara AJ, Nicholls PK, Warren KS, Friend JA & Swan RA (2007) Klossiella quimrensis (Apicomplexa: Klossiellidae) causes renal coccidiosis in western barred bandicoots Perameles bougainville (Marsupialia: Peramelidae) in Western Australia. Journal of Parasitology 93(1):89-92.
  • Bennett MD, Woolford L, O’Hara AJ, Nicholls PK, Warren KS, Swan RA, Friend JA, Hulme-Moir KL & Clark P (2007) Haematological characteristics of captive western barred bandicoots Perameles bougainville (Marsupialia: Peramelidae) from Western Australia. Veterinary Clinical Pathology. 36(4): 348-53.
  • Bennett MD, Woolford L, O’Hara AJ, Nicholls PK, Warren K & Hobbs RP (2006) A new eimeria species parasitic in western barred bandicoots, Perameles bougainville (Marsupialia: Peramelidae), in Western Australia. Journal of Parasitology 92(6):1292-4.

Conferences

  • Woolford L, Rector A, Van Ranst M, Ducki A, Bennett MD, Nicholls PK, Warren KS, Swan RA, Wilcox GE & O’Hara AJ (2007). A novel virus detected in papillomatous and carcinomatous lesions of the endangered western barred bandicoot (Perameles bougainville) exhibits genomic features of both the Papillomaviridae and Polyomaviridae. 24th International Papillomavirus Conference and Clinical Workshop. Beijing, China.
  • Woolford L, Rector A, Van Ranst M, Ducki A, Bennett MD, Nicholls PK, Warren KS, Swan RA, Wilcox GE & O’Hara AJ. A novel virus is detected in cutaneous papillomas and carcinomas of the western barred bandicoot (Perameles bougainville). Combined Biological Sciences Meeting, University of Western Australia, Western Australia, Australia, August 2007. Awarded Australian Society of Microbiology prize for best student poster.
  • Woolford L, Bennett MD, Warren KS Nicholls PK & O’Hara AJ. Frequency and distribution of a papillomatosis and carcinomatosis syndrome in the western barred bandicoot (Perameles bougainville). Annual meeting of the Australasian Wildlife Disease Association, Dryandra, Western Australia, Australia, September 2007
  • Woolford L, Bennett MD, Ducki A, Swan R, Nicholls PK, Warren KS & O’Hara AJ. Conservation, health and disease in the western barred bandicoot (Perameles bougainville). Wildlife Diseases Symposium, Perth Zoo, Western Australia, Australia, June 2007
  • Woolford L, O’Hara AJ, Rector A, Ducki A, Bennett MD, Warren KS, Swan RA, Sims C, Hill S, Nicholls PK, Friend JA & Van Ranst M. Detection of a novel papillomavirus in the highly endangered western barred bandicoot (Perameles bougainville) in association with a debilitating papillomatosis and carcinomatosis syndrome. Annual meeting of the Australian Association of Veterinary Laboratory Diagnosticians, Taronga Zoo, NSW, October 2006

Collaborators

Dr Annabel Rector and Professor Marc Van Ranst of the Laboratory of Clinical and Epidemiological Virology, Rega Institute for Medical Research, University of Leuven, Leuven, Belgium

Acknowledgements

This project was funded by the Australian Research Council in partnership with Murdoch University and the Western Australian Department of Environment and Conservation (DEC) under Linkage Project LP0455050. My candidature was funded by the Lorna Edith Murdoch Veterinary Trust Scholarship and assisted by the Murdoch Veterinary Trust Weston Fernie Scholarship.

Photos provided by Lucy Woolford

Department of Environment and ConservationAustralian Government | Australian Research CouncilKayana Wild Life