Papillomas and probable in situ carcinoma in association with a novel papillomavirus in a red-billed gull (Chroicocephalus novaehollandiae scopulinus)

Abstract

Numerous raised plaques were observed on the feet of a red-billed gull (Chroicocephalus novaehollandiae scopulinus) that had been found dead. The plaques consisted of thickened epidermis with cell changes indicative of papillomavirus (PV) infection prominent within affected areas. Evidence suggesting progression to neoplasia was visible in one lesion. A DNA sequence that was most similar, but only 68.3% identical, to duck PV type 3 was amplified from the papillomas, suggesting a novel PV type. Lesions containing PV DNA have only previously been reported in three avian species. This is the first evidence that PVs could cause neoplasia in birds.

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References

  1. 1.

    Bernard HU, Burk RD, Chen Z, van Doorslaer K, Hausen H, de Villiers EM (2010) Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401:70–79

    CAS  Article  Google Scholar 

  2. 2.

    Canuti M, Munro HJ, Robertson GJ, Kroyer ANK, Roul S, Ojkic D, Whitney HG, Lang AS (2019) New insight into avian papillomavirus ecology and evolution from characterization of novel wild bird papillomaviruses. Front Microbiol 10:701

    Article  Google Scholar 

  3. 3.

    Daoust P-Y, Wadowska D, Kibenge F, Campagnoli RP, Latimer KS, Ritchie BW (2000) Proliferative pododermatitis associated with virus-like particles in a northern gannet. J Wildl Dis 36:378–382

    CAS  Article  Google Scholar 

  4. 4.

    Di Francesco CE, Profeta F, Romanucci M, Zuccarini R, Altea T, Malatesta D, Della Salda L, Marsilio F (2019) Evidence of avian poxvirus and papillomavirus infection in Gyps fulvus in Italy. Arch Virol 164:291–295

    Article  Google Scholar 

  5. 5.

    Doorbar J (2005) The papillomavirus life cycle. J Clin Virol 32(Suppl 1):S7-15

    CAS  Article  Google Scholar 

  6. 6.

    Gaynor AM, Fish S, Duerr RS, Cruz FN Jr, Pesavento PA (2015) Identification of a novel papillomavirus in a Northern Fulmar (Fulmarus glacialis) with viral production in cartilage. Vet Pathol 52:553–561

    CAS  Article  Google Scholar 

  7. 7.

    Jacobson ER, Mladinich CR, Clubb S, Sundberg JP, Lancaster WD (1983) Papilloma-like virus infection in an African gray parrot. J Am Vet Med Assoc 183:1307–1308

    CAS  PubMed  Google Scholar 

  8. 8.

    Jones AL, Suárez-Bonnet A, Mitchell JA, Ramirez GA, Stidworthy MF, Priestnall SL (2020) Avian papilloma and squamous cell carcinoma: a histopathological, immunohistochemical and virological study. J Comp Pathol 175:13–23

    CAS  Article  Google Scholar 

  9. 9.

    Lawson B, Robinson RA, Fernandez JR, John SK, Benitez L, Tolf C, Risely K, Toms MP, Cunningham AA, Williams RAJ (2018) Spatio-temporal dynamics and aetiology of proliferative leg skin lesions in wild British finches. Sci Rep 8:14670

    Article  Google Scholar 

  10. 10.

    Li Y, Meyer H, Zhao H, Damon IK (2010) GC content-based pan-pox universal PCR assays for poxvirus detection. J Clin Microbiol 48:268–276

    CAS  Article  Google Scholar 

  11. 11.

    Munday JS (2014) Bovine and human papillomaviruses: a comparative review. Vet Pathol 51:1063–1075

    CAS  Article  Google Scholar 

  12. 12.

    Munday JS, Thomson NA, Luff JA (2017) Papillomaviruses in dogs and cats. Vet J 225:23–31

    Article  Google Scholar 

  13. 13.

    Munday JS, MacLachlan CB, Perrott MR, Aberdein D (2019) Papillomavirus DNA is not amplifiable from bladder, lung, or mammary gland cancers in dogs or cats. Animals (Basel) 9:668

    Article  Google Scholar 

  14. 14.

    Tachezy R, Rector A, Havelkova M, Wollants E, Fiten P, Opdenakker G, Jenson AB, Sundberg JP, Van Ranst M (2002) Avian papillomaviruses: the parrot Psittacus erithacus papillomavirus (PePV) genome has a unique organization of the early protein region and is phylogenetically related to the chaffinch papillomavirus. BMC Microbiol 2:19

    Article  Google Scholar 

  15. 15.

    Truchado DA, Williams RAJ, Benítez L (2018) Natural history of avian papillomaviruses. Virus Res 252:58–67

    CAS  Article  Google Scholar 

  16. 16.

    Williams RAJ, Tolf C, Waldenström J (2018) Molecular identification of papillomavirus in ducks. Sci Rep 8:9096

    Article  Google Scholar 

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Acknowledgements

The authors would like to acknowledge the roles of Michele MacKenzie of Snells Beach, John O’Connell, Ministry for Primary Industries Surveillance and Incursion Investigation, Wallaceville, and the Vet Farm & Pet Clinic Warkworth in submitting the gull.

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This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Correspondence to John S. Munday.

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Munday, J.S., Hardcastle, M.R., Hunter, S. et al. Papillomas and probable in situ carcinoma in association with a novel papillomavirus in a red-billed gull (Chroicocephalus novaehollandiae scopulinus). Arch Virol 166, 1157–1161 (2021). https://doi.org/10.1007/s00705-021-04967-6

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