Advertisement

Bovine papilloma: aetiology, pathology, immunology, disease status, diagnosis, control, prevention and treatment: a review

  • Iniobong Chukwuebuka Ikenna Ugochukwu
  • Chioma Inyang Aneke
  • Idoko Sunday Idoko
  • Nuhu Abdulazeez Sani
  • Adole Jolly Amoche
  • Wayuta Philip Mshiela
  • Richard Emmanuel Ede
  • Najume Dogowar Giginya Ibrahim
  • Celestine Ibe O. Njoku
  • Anthony Kojo Beku Sackey
Review Article
  • 56 Downloads

Abstract

Bovine papillomavirus (BPV) induces diseases of economic and veterinary importance leading to significant economic losses to livestock owners such as leather depreciation and mortality when it progresses to neoplasms. BPV affects the spinosum and granulosum layers of the skin causing warts. There are many reportage of BPV infection in domestic animals such as cattle, birds and wild animals such as tapir, giraffe, antelope and zebras. It also causes equine sarcoids in horses and donkeys. Gross lesions seen are mainly benign papillomas which most times regress but occasionally persist and progress to malignancy of the urinary bladder and upper alimentary tract leading to Enzootic haematuria. Equine sarcoids could be of the occult, nodular or verrucous types. Due to the ability to BPV to cause cancers, haematuria and skin pathologies, diagnosis of this infection has attracted huge interests. Diagnostic techniques include clinical examination, histopathology, polymerase chain reaction (PCR) Southern blot, dot blot, reverse blot, in situ hybridization and immunohistochemistry. All the aforementioned have been very helpful in the diagnosis of BPV. In conclusion, this review focused on the aetiology, viral structure pathogenicity, transmission, macroscopic and microscopic pathology, pathogenesis, immunology, gene products, prevention, treatment and control of this virus in affected animal species.

Keywords

Bovine papillomavirus Mastitis Neoplasia Papillomatosis Sarcoids 

Notes

Acknowledgements

A special thanks goes to Prof E.I. Ugochukwu and Late (Dr) Majiyagbe for their helpful contributions and suggestions.

Author’s contributions

Ibrahim NDG, Njoku COI and Sackey AKB conceived the idea; Ugochukwu ICI, Aneke CI, Sani NA and Ede ER wrote the manuscript whilst Idoko SI, Adole JA and Mshielia WP made significant intellectual contributions. All Authors read and approved the manuscript for submission.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This review article does not contain any studies with animals or human participants performed by the author.

References

  1. Ackermann MR (2012) Sarcoids of horses. In: Zachary JF, McGavin MD (eds) Pathologic basis of veterinary disease, 5th edn. Elsevier Mosby, St. Louis, p 125Google Scholar
  2. Al-Ani FK, Al-Rawashdeh OF, Hailat NK, Shotar A (2000) Cutaneous papillomatosis in horses: response of horses to autogenous wart vaccine. Pak Vet J 20(4):163–165Google Scholar
  3. Alberti A, Pirino S, Pintore F, Addis MF, Chessa B, Cacciotto C, Cubeddu T, Anfossi A, Benenati G, Coradduzza E, Lecis R, Antuofermo E, Carcangiu L, Pittau M (2010) Ovis aries papillomavirus 3: a prototype of a novel genus in the family papillomaviridae associated with ovine squamous cell carcinoma. Virology 407:352–359CrossRefPubMedGoogle Scholar
  4. Alcântara BK, Alfieri AA, Headley SA, Rodrigues WB, RAA O, Lunardi M, Alfieri AF (2015) Molecular characterisation of bovine deltapapillomavirus (BPV1, 2 and 13) DNA in equine sarcoids. Pesqui Vet Bras 35(5):431–436CrossRefGoogle Scholar
  5. Anderson RA, Scobie L, O’Neil BW, Grindlay GJ, Campo MS (1997) Viral proteins of bovine papillomavirus type 4 during the development of alimentary canal tumours. Vet J 154:69–78CrossRefPubMedGoogle Scholar
  6. Anjos BL, Silva MS, Diefenbach A, Brito MF, Seppa GS, Brum MCS (2010) Sarcoide equino associado ao papilomavírus bovino BR-UEL-4. Ciênc Rural 40:1456–1459CrossRefGoogle Scholar
  7. Araldi RP, Melo TC, Diniz N, Carvalho RF, Beçak W, Stocco RC (2013) Bovine papillomavirus clastogenic effect analyzed in comet assay. Biomed Res Int 2013:1–7.  https://doi.org/10.1155/2013/630683 CrossRefGoogle Scholar
  8. Araldi RP, Melo TC, Neves AC, Spadacci-Morena DD, Magnelli RF, Modolo DG, de-Sá-Júnior PL, Mazucchelli-de-Souza J, Carvalh RF, Beçak W, Stocco RC (2015) Hyperproliferative action of bovine papillomavirus: genetic and histopathological aspects. Genet Mol Res 14(4):12942–12954CrossRefPubMedGoogle Scholar
  9. Ataseven VS, Kanat O, Ergun Y (2016) Molecular identification of bovine papillomaviruses in dairy and beef cattle: first description of Xi- and Epsilonpapillomavirus in Turkey. Turk J Vet Anim Sci 40:757–763CrossRefGoogle Scholar
  10. Bernard HU, Burk RD, Chen Z, van Doorslaer K, zur Hausen H, de Villiers EM (2010) Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401:70–79CrossRefPubMedPubMedCentralGoogle Scholar
  11. Betiol JC, Kignel S, Tristao W, Arruda AC, Santos SK, Barbieri R et al (2012) HPV 18 prevalence in oral mucosa diagnosed with verrucous leukoplakia: cytological and molecular analysis. J Clin Pathol 65:769–770CrossRefPubMedGoogle Scholar
  12. Bloch N, Breen M, Spradbrow PB (1994) Genomic sequences of bovine papillomaviruses in formalin-fixed sarcoids from Australian horses revealed by polymerase chain reaction. Vet Microbiol 41:163–172CrossRefPubMedGoogle Scholar
  13. Bogaert L, Van Poucke M, De Baere C, Dewulf J, Peelman L, Ducatelle R, Gasthuys F, Martens A (2007) Bovine papillomavirus load and mRNA expression, cell proliferation and p53 expression in four clinical types of equine sarcoid. J Gen Virol 88:2155–2161CrossRefPubMedGoogle Scholar
  14. Bogaert L, Martens A, Van Poucke M, Ducatelle R, De Cook H, Dewulf J, De Baere C, Peelman L, Gasthuys F (2008) High prevalence of bovine papillomaviral DNA in normal skin of equine sarcoid-affected and healthy horses. Vet Microbiol 129:58–68CrossRefPubMedGoogle Scholar
  15. Boiron M, Levy JP, Thomas M, Friedmann JC, Bernard J (1964) Some properties of bovine papilloma virus. Nature 201:423–424CrossRefPubMedGoogle Scholar
  16. Börkü MK, Atalay O, Kibar M, Cam Y, Atasever A (2007) Ivermectin is an effective treatment for bovine cutaneous papillomatosis. Res Vet Sci 83(3):360–363CrossRefPubMedGoogle Scholar
  17. Borzacchiello G (2007) Bovine papillomavirus infections in animals. In: Méndez-Vilas A (ed) Communicating current research and educational topics and trends in applied microbiology. pp 673–679Google Scholar
  18. Borzacchiello G, Roperto F (2008) Bovine papillomaviruses, papillomas and cancer in cattle. Vet Res 39(5):1–10CrossRefGoogle Scholar
  19. Brandt S, Schoster A, Tober E, Kainzbauer C, Burgstaller JP, Haralambus R, Steinborn E, Hinterhofer C, Stanek C (2011) Consistent detection of bovine papillomavirus in lesions, intact skin and peripheral blood mononuclear cells of horses affected by hoof canker. Equine Vet J 43:202–209CrossRefPubMedGoogle Scholar
  20. Bravo IG, de Sanjosé S, Gottschling M (2010) The clinical importance of understanding the evolution of papillomaviruses. Trends Microbiol 18(10):432–438CrossRefPubMedGoogle Scholar
  21. Campo MS (1988) Viral and cellular oncogenes in papilloma virus associated cancers. Brit J Canc Suppl 9:80–84Google Scholar
  22. Campo MS (1997) Bovine papillomavirus and cancer. Vet J 154:175–188CrossRefPubMedGoogle Scholar
  23. Campo MS (1998) Persistent infection by bovine papillomavirus. In: Ahmed R (ed) Persistent viral infections. John Wiley and Sons, Sussex, pp 503–516Google Scholar
  24. Campo MS (2002) Animal models of papillomavirus pathogenesis. Virus Res 89(2):249–261CrossRefPubMedGoogle Scholar
  25. Campo MS (2006) Bovine papillomavirus: old system, new lessons? In: Campo MS (ed) Papillomavirus research: from natural history to vaccine and beyond. Caister Academic Press, Wymondham, pp 1–31Google Scholar
  26. Carr EA, Theon AP, Madewell BR, Griffey SM, Hitchcock ME (2001a) Bovine papillomavirus DNA in neoplastic and non-neoplastic tissues obtained from horses with and without sarcoids in the western United States. Am J Vet Res 62:741–744CrossRefPubMedGoogle Scholar
  27. Carr EA, Theon AP, Madewell BR, Hitchcock ME, Schlegel R, Schiller JT (2001b) Expression of a transforming gene (E5) of bovine papillomavirus in sarcoids obtained from horses. Am J Vet Res 62:1212–1217CrossRefPubMedGoogle Scholar
  28. Catroxo M, Martins A, Petrella S, Souza F, Nastari B (2013) Ultrastructural study of bovine papillomavirus during outbreaks in Brazil. Int J Morphol 31:777–784CrossRefGoogle Scholar
  29. Chambers G, Ellsmore VA, O’Brien PM, Reid SWJ, Love S, Campo MS, Nasir L (2003) Sequence variants of bovine papillomavirus E5 detected in equine sarcoids. Virus Res 96:141–145CrossRefPubMedGoogle Scholar
  30. Chow LT, Broker TR (2006) Mechanisms and regulation of papillomavirus DNA replication. In: Campo MS (ed) Papillomavirus research: from natural history to vaccines and beyond. Caister Academic Press, Norfolk, pp 53–71Google Scholar
  31. Claus MP, Lunardi M, Alfieri AA, Otonel RAA, Sartori D, Fungaro MHP, Alfieri AF (2009) Multiple bovine papillomavirus infections associated with cutaneous papillomatosis in Brazilian cattle herds. Braz Arch Biol Technol 52:93–98CrossRefGoogle Scholar
  32. Dagalp SB, Dogan F, Farzani TA, Salar S, Bastan A (2017) The genetic diversity of bovine papillomaviruses (BPV) from different papillomatosis cases in dairy cows in Turkey. Arch Virol 162(6):1507–1518CrossRefPubMedGoogle Scholar
  33. De Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H (2004) Classification of papillomaviruses. Virology 324:17–27CrossRefPubMedGoogle Scholar
  34. De Villiers EM (2013) Cross-roads in the classification of papillomaviruses. Virology 445:2–10CrossRefPubMedGoogle Scholar
  35. Elzein ET, Sundberg JP, Housawi FM, Gameel AA, Ramadan RO, Hassanein MM (1991) Genital bovine papillomavirus infection in Saudi Arabia. J Vet Diagn Investig 3:36–38CrossRefGoogle Scholar
  36. Finlay M, Yuan Z, Burden F, Trawford A, Morgan IM, Campo MS, Nasir L (2009) The detection of bovine papillomavirus type 1 DNA in flies. Virus Res 144:315–317CrossRefPubMedGoogle Scholar
  37. Finlay M (2011) Equine sarcoids and bovine papillomavirus: unraveling the viral pathogenesis. Dissertation, University of Glasgow. GlasgowGoogle Scholar
  38. Freitas AC, Carvalho C, Brunner O, Birgel EH Jr, Libera AMD, Benesi FJ, Beçak W, Stocco dos Santos RC (2003) Viral DNA sequences in peripheral blood and vertical transmission of the vírus: a discussion about BPV-1. Braz J Microbiol 34:76–78CrossRefGoogle Scholar
  39. Freitas AC, Silva MAR, Carvalho CCR, Birgel EH Jr, Santos JF, Beçak W, Stocco dos Santos RC (2007) Papillomavirus DNA detection in non-epithelial tissues: a discussion about bovine papillomavirus. In: Mendez-Villas A (ed) Communicating current research and educational topics and trends in applied microbiology. Formatex, Badajos, pp 697–704Google Scholar
  40. Ginn PE, Mansell JEKL, Rakich PM (2007) Skin and appendages. In: Maxie MG (ed) Jubb, Kennedy, and Palmer’s pathology of domestic animals, vol 1. Saunders/Elsevier, Philadelphia, pp 748–751Google Scholar
  41. Gourreau J, Bendali F (2008) The papillomatosis. In F Agricole (ed) Diseases of cattle. 376–379Google Scholar
  42. Grindatto A, Ferraro G, Varello K, Crescio MI, Miceli I, Bozzetta E, Goria M, Nappi R (2015) Molecular and histological characterisation of bovine papillomavirus in North West Italy. Vet Microbiol 180(1–2):113–117CrossRefPubMedGoogle Scholar
  43. Hamad MA, Al-Shammari AM, Odisho SM, Yaseen NY (2016) Molecular and phylogenetic analysis of bovine papillomavirus type 1: first report in Iraqi cattle. Adv Virol 2016:1–7.  https://doi.org/10.1155/2016/2143024 CrossRefGoogle Scholar
  44. Hargis AM, Ginn PE (2012) The integument. In: Zachary JF, McGavin MD (eds) Pathologic basis of veterinary disease, 5th ed. Elsevier/Mosby, St. Louis, pp. 1025–1027Google Scholar
  45. Hatama S (2012) Cutaneous papillomatosis in cattle. J Disaster Res 7(3):319–323CrossRefGoogle Scholar
  46. Jagu S, Malandro N, Kwak K, Yuan H, Schlegel R, Palmer KE, Huh WK, Campo MS, Roden RB (2011) A multimeric L2 vaccine for prevention of animal papillomavirus infections. Virology 420(1):43–50CrossRefPubMedPubMedCentralGoogle Scholar
  47. Jarrett WFH, O’Neil BW, Gaukroger JM, Smith KT, Laird HM, Campo MS (1990) Studies on vaccination against papillomaviruses: the immunity after infection and vaccination with bovine papillomaviruses of different types. Vet Rec 126:473–475PubMedGoogle Scholar
  48. Jeremiah OT, Fagbohun OA, Babalola OJ (2016) Molecular detection of bovine papilloma viruses associated with cutaneous warts in some breeds of Nigerian cattle. Int J Biotech Biochem 12(2):123–130Google Scholar
  49. Kidney BA, Berrocal A (2008) Sarcoids in two captive tapirs (Tapirus bairdii): clinical, pathological and molecular study. Vet Dermatol 19(6):380–384CrossRefPubMedGoogle Scholar
  50. Kirnbauer R, Booy F, Cheng N, Lowy DR, Schiller JT (1992) Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc Natl Acad Sci U S A 89:12180–12184CrossRefPubMedPubMedCentralGoogle Scholar
  51. Kirnbauer R, Chandrachud LM, O’Neil BW, Wagner ER, Grindlay GJ, Armstrong A, McGarvie GM, Schiller JT, Lowy DR, Campo MS (1996) Virus-like particles of bovine papillomavirus type 4 in prophylactic and therapeutic immunization. Virology 219:37–44CrossRefPubMedGoogle Scholar
  52. Lesnik F, Bires J, Suli J, Posivak J, Mattova J, Svrcek S, Sevcikova Z, Kvokacka V, Gaspar V, Levkut M, Buleca J (1999) Autovaccination and metabolic profiles at bovine papillomatosis. Slov Vet J 24:290–294Google Scholar
  53. Leto M, Santos Júnior GF, Porro AM, Tomimori J (2011) Human papillomavirus infection: etiopathogenesis, molecular biology and clinical manifestations. An Bras Dermatol 86:306–317CrossRefPubMedGoogle Scholar
  54. Lindsey CL, Almeida ME, Vicari CF, Carvalho C, Yaguiu A, Freitas AC, Beçak W, Stocco dos Santos RC (2009) Bovine papillomavirus DNA in milk, urine, semen and spermatozoa of BPV infected animals. Genet Mol Res 8:310–318CrossRefPubMedGoogle Scholar
  55. Littlewood JD, Heidmann P (2006) The skin. In: Higgins AJ, Snyder JR (eds) The equine manual, 2nd edn. Elsevier, London, pp 305–359CrossRefGoogle Scholar
  56. Löhr CV, Juan-Sallés C, Rosas-Rosas A, Parás García A, Garner MM, Teifke JP (2005) Sarcoids in captive zebras (Equus burchellii): association with bovine papillomavirus type 1 infection. J Zoo Wildlife Med 36(1):74–81CrossRefGoogle Scholar
  57. Lucena RB, Rissi DR, Kommers GD, Pierezan F, Oliveira-Filho JC, Macêdo JT, Flores MM, Barros CS (2011) A retrospective study of 586 tumours in Brazilian cattle. J Comp Pathol 145(1):20–24CrossRefPubMedGoogle Scholar
  58. Lunardi M, de Alcântara BK, Otonel RAA, Rodrigues WB, Alfieri AF, Alfieri AA (2013) Bovine papillomavirus type 13 DNA in equine sarcoids. J Clin Microbiol 51:2167–2171CrossRefPubMedPubMedCentralGoogle Scholar
  59. Marins RSQS, Ferreira CEP (2011) Clinicopathologic and epithelial regression study in cutaneous warts of bovines infected by papillomavirus. Int Res J Pharm Pharmacol 1:12–16Google Scholar
  60. Mariz FC, Jesus ALS, Silva MAR (2016) The challenges inherent in the control and prevention of bovine papillomaviruses. Austin J Genet Genom Res 3(1):10–17Google Scholar
  61. Martens A, De Moor A, Demeulemeester J, Peelman L (2001a) Polymerase chain reaction analysis of the surgical margins of equine sarcoids for bovine papilloma virus DNA. Vet Surg 30:460–467CrossRefPubMedGoogle Scholar
  62. Martens A, De Moor A, Ducatelle R (2001b) PCR detection of bovine papilloma virus DNA in superficial swabs and scrapings from equine sarcoids. Vet J 161:280–286CrossRefPubMedGoogle Scholar
  63. Modis Y, Trus BL, Harrison SC (2002) Atomic model of the papillomavirus capsid. EMBO J 21:4754–4762CrossRefPubMedPubMedCentralGoogle Scholar
  64. Munday JS, Knight CG (2010) Amplification of feline sarcoid-associated papillomavirus DNA sequences from bovine skin. Vet Dermatol 21:341–344CrossRefPubMedGoogle Scholar
  65. Munday JS (2014) Bovine and human papillomaviruses: a comparative review. Vet Pathol 51(6):1063–1075Google Scholar
  66. Nasir L, Campo MS (2008) Bovine papillomaviruses: their role in the aetiology of cutaneous tumors of bovids and equids. Vet Dermatol 19:243–254CrossRefPubMedGoogle Scholar
  67. Nasir L, Brandt S (2013) Papillomavirus associated diseases of the horse. Vet Microbiol 167:159–167CrossRefPubMedGoogle Scholar
  68. Nicholls PK, Stanley MA (2000) The immunology of animal papillomaviruses. Vet Immunol Immunopathol 75(2):101–127CrossRefGoogle Scholar
  69. Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, Amino N, Hase T (2001) Loop-mediated isothermal amplification of DNA. Nucleic Acids Res 28(12):E63CrossRefGoogle Scholar
  70. Ogawa T, Tomita Y, Okada M, Shinozaki HK, Kaiho I, Shirasawa H (2004) Broad-spectrum detection of papillomaviruses in bovine teat papillomas and health teat skin. J Gen Virol 85:2191–2197CrossRefPubMedGoogle Scholar
  71. Olson C Jr, Cook RH (1951) Cutaneous sarcoma-like lesions of the horse caused by the agent of bovine papilloma. Proc Soc Exp Biol Med 77:281–284CrossRefPubMedGoogle Scholar
  72. Otten N, von Tscharner C, Lazary SD, Antczak F, Gerber H (1993) DNA of bovine papillomavirus type 1 and 2 in equine sarcoids: PCR detection and direct sequencing. Arch Virol 132:121–131CrossRefPubMedGoogle Scholar
  73. Pangty K, Singh S, Goswami R, Saikumar G, Somvanshi R (2010) Detection of BPV-1 and -2 and quantification of BPV-1 by real-time PCR in cutaneous warts in cattle and buffaloes. Transbound Emerg Dis 57:185–196CrossRefPubMedGoogle Scholar
  74. Pascoe RRR, Knottenbelt DC (1999) Neoplastic conditions. In: Pascoe RRR, Knottenbelt DC (eds) Manual of equine dermatology. WB Saunders, London, pp 244–252Google Scholar
  75. Postey RC, Appleyard GD, Kidney BA (2007) Evaluation of equine papillomas, aural plaques, and sarcoids for the presence of Equine papillomavirus DNA and Papillomavirus antigen. Can J Vet Res 71(1):28–33PubMedPubMedCentralGoogle Scholar
  76. Radostits OM, Gay CC, Hinchcliff HW, Constable PD (2006) Viral diseases characterized by skin lesions. In: Radostits OM, Gay CC, Hinchcliff HW, Constable PD (eds) Veterinary medicine: a textbook of the diseases of cattle, horses, sheep, pigs and goats, 10th edn. Saunders Elsevier, Edinburgh, pp 1421–1422Google Scholar
  77. Rees CA (2004) Disorders of the skin. In: Reed SM, Bayly WM, Sellon DC (eds) Equine Internal Medicine, 2nd edn, St. Louis, pp 667–720Google Scholar
  78. Robl MG, Olson C (1968) Oncogenic action of bovine papilloma virus in hamsters. Cancer Res 28:1596–1604PubMedGoogle Scholar
  79. Roperto S, Russo V, Ozkul A, Corteggio A, Sepici-Dincel A, Catoi C, Esposito I, Riccardi MG, Urraro C, Lucà R, Ceccarelli DM, Longo M, Roperto F (2013) Productive infection of bovine papillomavirus type 2 in the urothelial cells of naturally occurring urinary bladder tumors in cattle and water buffaloes. PLoS One 8(5):e62227CrossRefPubMedPubMedCentralGoogle Scholar
  80. Schmitt M, Fiedler V, Muller M (2010) Prevalence of BPV genotypes in a German cowshed determined by a novel multiplex BPV genotyping assay. J Virol Methods 170:67–72CrossRefPubMedGoogle Scholar
  81. Shah KV, Howley PM (1996) Papillomaviruses. In: Fields virology, 3rd edn. Lippincott - Raven Publishers, Philadelphia, pp 2077–2101Google Scholar
  82. Silvestre O, Borzacchiello G, Nava D, Iovane G, Russo V, Vecchio D, D’Ausilio F, Gault EA, Campo MS, Paciello O (2009) Bovine papillomavirus type 1 DNA and E5 oncoprotein expression in water buffalo fibropapillomas. Vet Pathol 46:636–641CrossRefPubMedGoogle Scholar
  83. Stocco dos Santos RC, Lindsey CJ, Ferraz OP, Pinto JR, Mirandola RS, Benesi FJ, Birgel EH, Pereira CA, Beçak W (1998) Bovine papillomavirus transmission and chromosomal aberrations: an experimental model. J Gen Virol 79(9):2127–2135CrossRefPubMedGoogle Scholar
  84. Sundberg JP (1987) Papillomavirus infections in animals. In: Syrjanen K, Gissmann L, Koss L (eds) Papillomaviruses and human disease. Springer-Verlag, Heidelberg, pp 40–103CrossRefGoogle Scholar
  85. Sundberg JP, VanRanst M, Burk RD, Jenson AB (1996) The nonhuman (animal) papillomaviruses: host range, epitope conservation, and molecular diversity. In: Gross G, von Krogh G (eds) Human papillomavirus infections in dermatology and venereology. CRC Press, Boca Raton, pp 47–68Google Scholar
  86. Teifke JP, Hardt M, Weiss E (1994) Detection of bovine papillomavirus DNA in formalin-fixed paraffin-embedded equine sarcoids by polymerase chain reaction and non-radioactive in situ hybridization. Eur J Vet Pathol 1:5–10Google Scholar
  87. Timurkan MO, Alcigir ME (2017) Phylogenetic analysis of a partial L1 gene from bovine papillomavirus type 1 isolated from naturally occurring papilloma cases in the northwestern region of Turkey. Onders J Vet Res 84(1):a1450.  https://doi.org/10.4102/ojvr.v84i1.1450 CrossRefGoogle Scholar
  88. Tomita Y, Literak I, Ogawa T, Jin Z, Shirasawa H (2007) Complete genomes and phylogenetic positions of bovine papillomavirus type 8 and a variant type from a European bison. Virus Genes 35(2):243–249CrossRefPubMedGoogle Scholar
  89. Tomita N, Mori Y, Kanda H, Notomi T (2008) Loop-mediated isothermal amplification (LAMP) of gene sequences and simple visual detection of products. Nat Protoc 3:877–882CrossRefPubMedGoogle Scholar
  90. Tozato CC, Lunardi M, Alfieri AF, Otonel RAA, Di Santis GW, de Alcântara BK, Headley SA, Alfieri AA (2013) Teat papillomatosis associated with bovine papillomavirus types 6, 7, 9, and 10 in dairy cattle from Brazil. Braz J Microbiol 44(3):905–909CrossRefPubMedPubMedCentralGoogle Scholar
  91. Trewby H, Ayele G, Borzacchiello G, Brandt S, Campo MS, Del Fava C, Marais J, Leonardi L, Vanselow B, Biek R, Nasir L (2014) Analysis of the long control region of bovine papillomavirus type 1 associated with sarcoids in equine hosts indicates multiple cross-species transmission events and phylogeographical structure. J Gen Virol 95(12):2748–2756CrossRefPubMedPubMedCentralGoogle Scholar
  92. Tsirimonaki E, O’Neil BW, Williams R, Campo MS (2003) Extensive papillomatosis of the bovine upper gastrointestinal tract. J Comp Pathol 29:93–99CrossRefGoogle Scholar
  93. Turk N, Župančić Z, Starešina V, Kovač S, Babić T, Kreszinger M, Ćurić S, Barbić L, Milas Z (2005) Severe bovine papillomatosis: detection of bovine papillomavirus in tumour tissue and efficacy of treatment using autogenous vaccine and parammunity inducer. Vet Arhiv 75(5):391–397Google Scholar
  94. Ugochukwu ICI (2018) Bracken fern toxicity and its associated clinicopathological effects in humans and animals: a review. Comp Clin Pathol.  https://doi.org/10.1007/s00580-018-2636-2
  95. Williams H, Van Dyk E, Nela PJ, Lane E, Van Wilpe E, Bengis RG, de Klerk-Lorist LM, van Heerden J (2011) Pathology and immunohistochemistry of papillomavirus-associated cutaneous lesions in Cape mountain zebra, giraffe, sable antelope and African buffalo in South Africa. J South Afr Vet Ass 82(2):97–106Google Scholar
  96. Wobeser BK, Hill JE, Jackson ML, Kidney BA, Mayer MN, Townsend HGG, Allen AL (2012) Localization of Bovine papillomavirus in equine sarcoids and inflammatory skin conditions of horses using laser microdissection and two forms of DNA amplification. J Vet Diagn Invest 24(1):32–41CrossRefPubMedGoogle Scholar
  97. Wobeser BK (2016) Making the diagnosis equine sarcoid. Vet Pathol 0300985816664793Google Scholar
  98. Yaguiu A, Carvalho C, Freitas AC, Góes LGB, Dagli MLZ, Birgel EH Jr, Beçak W, Stocco dos Santos RC (2006) Papillomatosis in cattle: in situ detection of bovine papillomavirus DNA sequences in reproductive tissues. Bra J Morph Sci 23:525–529Google Scholar
  99. Yaguiu A, Dagli MLZ, Birgel EH Jr, Alves Resi BCAA, Ferraz OP, Goes LGB, Pituco EM, Freitas AC, Beçak W, Stocco do Santos RC (2008) Simultaneous presence of bovine papillomavirus (BPV) and bovine leukemia virus (BLV) in different bovine tissues: in situ hybridization and cytogenetic analysis. Genet Mol Res 7:487–497CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag London Ltd., part of Springer Nature 2018

Authors and Affiliations

  • Iniobong Chukwuebuka Ikenna Ugochukwu
    • 1
  • Chioma Inyang Aneke
    • 1
  • Idoko Sunday Idoko
    • 2
  • Nuhu Abdulazeez Sani
    • 2
  • Adole Jolly Amoche
    • 3
  • Wayuta Philip Mshiela
    • 4
  • Richard Emmanuel Ede
    • 4
  • Najume Dogowar Giginya Ibrahim
    • 5
  • Celestine Ibe O. Njoku
    • 5
  • Anthony Kojo Beku Sackey
    • 4
  1. 1.Department of Veterinary Pathology and MicrobiologyUniversity of Nigeria NsukkaNsukkaNigeria
  2. 2.Department of Veterinary PathologyUniversity of AbujaAbujaNigeria
  3. 3.Viral Research DivisionNational Veterinary Research InstituteVomNigeria
  4. 4.Department of Veterinary MedicineAhmadu Bello UniversityZariaNigeria
  5. 5.Department of Veterinary PathologyAhmadu Bello UniversityZariaNigeria

Personalised recommendations