Archives of Virology

, Volume 163, Issue 6, pp 1635–1642 | Cite as

A teat papillomatosis case in a Damascus goat (Shami goat) in Hatay province, Turkey: a new putative papillomavirus?

  • Fırat Dogan
  • Selvi Deniz Dorttas
  • Seval Bilge Dagalp
  • Veysel Soydal Ataseven
  • Feray Alkan
Original Article


Papillomaviruses (PVs) are epitheliotropic viruses that cause benign proliferative lesions in the skin (warts or papillomas) and mucous membranes of their natural hosts. Recently, new PVs have been found in many animal species. The most common current approach for identifying novel PV types is based on PCR, using various consensus or degenerated primer (broad-range primers), designed on the basis of the multiple alignment of nucleotide or amino acid sequences of a large number of different human papillomaviruses (HPV). PVs have been classified according to the sequence similarity of one of their capsid proteins, L1, without taking into account other regions of the genome and without considering the phenotypic characteristics of the viral infection. In this study, we performed molecular detection and typing of a PV in a goat with teat papillomatosis. Firstly, PCR was performed using the FAP59/FAP64 and MY09/MY11 primer pairs for the L1 gene region. The PV DNA was found to be positive only with the FAP59/FAP64 primer pair. PV DNA was then tested with three primer sets in four different combinations (L2Bf/FAP64, L2Bf/L1Br, FAP59/FAP64, L1Bf/LCRBr) for the gene region encoding the L1, L2 and LCR proteins. The goat teat papilloma sample was amplified using FAP59/FAP64 primers and two primer pairs (L2Bf/FAP64 and L2Bf/L1Br). We obtained products matching approximately 604 bp of the L1 region of the virus. PV DNA was used for typing using sequence analysis/PCR with some type-specific primers for bovids, caprids and cervids. The results of the sequence analysis suggested one new putative PV type with sequence identity ranging from 46.45 to 80.09% to other known papillomaviruses, including Capra hircus papillomavirus (ChPV-2), bovine papillomavirus (BPV) 6, 7, 10, 11 and 12, Rangifer tarandus papillomavirus 3 (RtPV-3) and BPV-7Z (Alpine wild ruminant papillomavirus; Cervus elaphus papillomavirus). We therefore propose that this is the first identification of a new putative type, MG523274 (HTY-goat-TR2016), in a goat with teat papillomatosis. It is essential to identify PV types in different animal species and investigate their prevalence/distribution and clinical consequences in order to develop appropriate prophylactic and/or therapeutic procedures and to determine the interspecies transmission potential and evolution of PVs.



We thank Vet. Ali Haciömeroglu for all of the help.


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

Compliance with ethical standards

Conflict of interest

All authors declare that there is no conflict of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Supplementary material

705_2018_3781_MOESM1_ESM.tif (46 kb)
Gel electrophoresis image after PCR with the FAP59/FAP64 primer pair (TIF 47 kb)


  1. 1.
    Altschul SF, Madden TL, Schäffer AA (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 17:3389–3402CrossRefGoogle Scholar
  2. 2.
    Antonsson A, Hansson BG (2002) Healthy skin of many animal species harbors papillomaviruses which are closely related to their human counterparts. J Virol 76:12537–12542CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Ataseven VS, Kanat Ö, Ergün Y (2016) Molecular identification of bovine papillomaviruses in dairy and beef cattle: first description of Xi- and Epsilonpapillomaviruses in Turkey. Turk J Vet Anim Sci 40(6):757–763CrossRefGoogle Scholar
  4. 4.
    Bernard HU, Burk RD, Chen Z, van Doorslaer K, Hause H, de Villiers EM (2010) Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401:70–79CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Bilge Dagalp S, Dogan F, Farzanı TA, Salar S, Bastan A (2017) The genetic diversity of bovine papillomaviruses (BPV) from different papillomatosis cases in dairy cows in Turkey. Arch Virol 162:1507–1518CrossRefGoogle Scholar
  6. 6.
    Bogaert L, Martens A, Kast W, Van Marck E, De Cock H (2010) Bovine papillomavirus DNA can be detected in keratinocytes of equine sarcoid tumors. Vet Microbiol 146:269–275CrossRefPubMedGoogle Scholar
  7. 7.
    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, Poole, United Kingdom, pp 373–387Google Scholar
  8. 8.
    Carvalho CCR, Batista MVA, Silva MAR, Balbino VQ, Freitas AC (2012) Detection of bovine papillomavirus types, co-infection and new BPV11 subtype in cattle. Transbound Emerg Dis 59:441–447CrossRefPubMedGoogle Scholar
  9. 9.
    Claus MP, Lunardi M, Alfieri AF (2009) Identification of the recently described new type of bovine papillomavirus (BPV-8) in a Brazilian beef cattle herd. Pesqui Vet Bras 29:25–28CrossRefGoogle Scholar
  10. 10.
    Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287(5452):443CrossRefPubMedGoogle Scholar
  11. 11.
    de Villiers EM, Fauquet C, Broker TR, Bernard HU, Hausen H (2004) Classification of papillomaviruses. Virology 1:17–27CrossRefGoogle Scholar
  12. 12.
    de Villiers E (2013) Cross-roads in the classification of papillomaviruses. Virology 445:2–10CrossRefPubMedGoogle Scholar
  13. 13.
    Erdélyi K, Bálint Á, Dencső L, Dán Á, Ursu K (2008) Characterisation of the first complete genome sequence of the roe deer (Capreolus capreolus) papillomavirus. Virus Res 135(2):307–311CrossRefPubMedGoogle Scholar
  14. 14.
    Forslund O, Antonsson A, Nordin P (1999) A broad range of human papillomavirus types detected with a general PCR method suitable for analysis of cutaneous tumours and normal skin. J Gen Virol 80:2437–2443CrossRefPubMedGoogle Scholar
  15. 15.
    Freitas AC, Silva MAR, Jesus ALS, Mariz FC, Cordeiro MN, Albuquerque BMF, Batista MVA (2011) Recent insights into bovine papillomavirus. Afr J Microbiol Res 5(33):6004–6012 (31) CrossRefGoogle Scholar
  16. 16.
    Gottschling M, Stamatakis A, Nindl I, Stockfleth E, Alonso A, Bravo IG (2007) Multiple evolutionary mechanisms drive papillomavirus diversification. Mol Biol Evol 24(5):1242–1258. (advance access publication March 6, 2007) CrossRefPubMedGoogle Scholar
  17. 17.
    Groff DE, Sundberg JP, Lancaster WD (1983) Extrachromosomal deer fibromavirus DNA in deer fibromas and virus-transformed mouse cells. Virology 131:545–550CrossRefGoogle Scholar
  18. 18.
    Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  19. 19.
    Jackson ME, Pennie WD, McCaffery RE, Smith KT, Grindlay GJ, Campo MS (1991) The B subgroup bovine papillomaviruses lack an identifiable E6 open reading frame. Mol Carcinog 4:382–387CrossRefPubMedGoogle Scholar
  20. 20.
    Kumar P, Nagarajan N, Saikumar G, Arya RS, Somvanshi R (2013) Detection of bovine papilloma viruses in wart-like lesions of upper gastrointestinal tract of cattle and buffaloes. Transbound Emerg Dis 63:56–67Google Scholar
  21. 21.
    Lambert PF, Baker CC, Howley PM (1988) The genetics of bovine papillomavirus type 1. Annu Rev Genet 22:235–258CrossRefPubMedGoogle Scholar
  22. 22.
    Lindsey CL, Almeida ME, Vicari CF, Carvalho C, Yaguiu A, Freitas AC, Becak W, Stocco RC (2009) Bovine papillomavirus DNA in milk, blood, urine, semen, and spermatozoa of bovine papillomavirus-infected animals. Genet Mol Res 8:310–318CrossRefPubMedGoogle Scholar
  23. 23.
    Literak I, Tomita Y, Ogawa T, Shirasawa H, Smid B, Novotny L, Adamec M (2006) Papilomatosis in a European bison. J Wildl Dis 42:149–153CrossRefPubMedGoogle Scholar
  24. 24.
    Löhr CV, Juan-Sallés C, Rosas-Rosas A, Parás García A, Garner MM, Teifk JP (2005) Sarcoids in captive zebras (Equus burchellii): association with bovine papillomavirus type 1 infection. J Zoo Wildl Med 36:74–81CrossRefPubMedGoogle Scholar
  25. 25.
    Lunardi M, Claus MP, Alfieri AA, Fungaro MHP, Alfieri AF (2010) Phylogenetic position of an uncharacterized Brazilian strain of bovine papillomavirus in the genus Xipapillomavirus based on sequencing of the L1 open reading frame. Genet Mol Biol 33(4):745–749CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Lunardi M, de Alcantara BK, Otonel RA, Rodrigues WB, Alfieri AF, Alfieri AA (2013) Bovine papillomavirus type 13 DNA in equine sarcoids. J Clin Microbiol 51:2167–2171CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Maiolino PA, Ozkul A, Sepici-Dincel A, Roperto F, Yucel G, RussoV Urraro C, Luca R, Riccardi MG, Martano M, Borzacchiello G, Esposito I, Roperto S (2013) Bovine papillomavirus type 2 infection and microscopic patterns of urothelial tumors of the urinary bladder in water buffaloes. Biomed Res Int 146:269–275Google Scholar
  28. 28.
    Manni V, Ropertob F, Di Guardoc G, Galatid D, Condoleoc RU, Venutia A (1998) Presence of papillomavirus-like DNA sequences in cutaneous fibropapillomas of the goat udder. Vet Microbiol 61(1–2):1–6CrossRefPubMedGoogle Scholar
  29. 29.
    Manos MM, Ting Y, Wright DK, Lewis AJ, Broker TR, Wolinsky SM (1989) The use of polymerase chain reaction amplification for the detection of genital human papillomaviruses. Cancer Cell 7:209–214Google Scholar
  30. 30.
    Mengual-Chulia B, Garcia-Perez R, Gottschling M, Nindl I, Bravo IG (2012) Novel animal papillomavirus sequences and accurate phylogenetic placement. Mol Phylogenet Evol 65:883–891CrossRefPubMedGoogle Scholar
  31. 31.
    Moreno-Lopez J, Pettersson U, Dinter Z, Philipson L (1981) Characterization of a papilloma virus from the European elk (EEPV). Virology 112:589–595CrossRefPubMedGoogle Scholar
  32. 32.
    Moreno-Lopez J, Ahola H, Eriksson A, Bergman P, Pettersson U (1987) Reindeer papillomavirus transforming properties correlate with a highly conserved E5 region. J Virol 61:3394–3400PubMedPubMedCentralGoogle Scholar
  33. 33.
    Moar MH, Jarrett WFH (1985) A cutaneous fibropapilloma from a red deer (Cervus elaphus) associated with a papillomavirus. Intervirology 24:108–118CrossRefPubMedGoogle Scholar
  34. 34.
    Munger K, Howley PM (2002) Human papillomavirus immortalization and transformation functions. Virus Res 89:213–228CrossRefPubMedGoogle Scholar
  35. 35.
    Munday JS, Knight CG (2010) Amplification of feline sarcoidassociated papillomavirus DNA sequences from bovine skin. Vet Dermatol 21:341–344CrossRefPubMedGoogle Scholar
  36. 36.
    Nasir L, Campo MS (2008) Bovine papillomaviruses: their role in the aetiology of cutaneous tumours of bovids and equids. Vet Dermatol 19:243–254CrossRefPubMedGoogle Scholar
  37. 37.
    Ogawa T, Tomita Y, Okada M, Schinozaki K, Kubonoya H, Kaiho I, Shirisawa H (2004) Broad-spectrum detection of papillomaviruses in bovine teat papillomas and healthy teat skin. J Gen Virol 85:2191–2197CrossRefPubMedGoogle Scholar
  38. 38.
    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
  39. 39.
    Rector A, Van Ranst M (2013) Animal papillomaviruses. Virology 445:213–223CrossRefPubMedGoogle Scholar
  40. 40.
    Roperto S, Russo V, Ozkul A, Corteggio A, Sepici-Dincel A, Catoi C, Esposito I, Riccardi MG, Urraro C, Luca 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:e62227CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Ruiz de Ybáñez MR, Martínez-Carrasco C, Alonso FD, León L (2009) Lungworm infection of wild ruminants in the Sierras de Cazorla, Segura and Villas Natural Park (Jaén, España). Acta Parasitol Port 16:184–185Google Scholar
  42. 42.
    Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, New YorkGoogle Scholar
  43. 43.
    Santos EUD, Silva MAR, Pontes NE, Coutinho LCA, Paiva SSL, Castro RS, Freitas AC (2016) Detection of different bovine papillomavirus types and co-infection in bloodstream of cattle. Transbound Emerg Dis 63:103–108CrossRefGoogle Scholar
  44. 44.
    Savini F, Gallina L, Alberti A, Müller M, Scagliarini A (2016) Bovine papillomavirus type 7 in Italy: complete genomes and sequence variants. Virus Genes 52(2):253–260CrossRefPubMedGoogle Scholar
  45. 45.
    Scagliarini A, Gallina L, Battilani M, Turrini F, Savini F, Lavazza A, Alberti A (2013) Cervus elaphus papillomavirus (CePV1): new insights on viral evolution in deer. Vet Microbiol 165(3):252–259CrossRefPubMedGoogle Scholar
  46. 46.
    Silva MS, Weiss M, Brum MCS, Anjos BL, Torres FD, Weiblen R, Flores EF (2010) Molecular identification of bovine papillomaviruses associated with cutaneous warts in southern Brazil. J Vet Diagn Investig 22:603–606CrossRefGoogle Scholar
  47. 47.
    Silvestre O, Borzacchiello G, Nava D, Iovane D, 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
  48. 48.
    Simeonea P, Romanuccib M, Rizzoa C, Brandia R, Malatestab D, Di Guardob G, Bongiovannib L, Salda LD, Venuti A (2008) Papillomaviruses in multiple tumours of twin goats. Open Vet Sci J 2:33–36CrossRefGoogle Scholar
  49. 49.
    Singh V, Somvanshi R, Tiwari AK (2009) Papillomatosis in Indian cattle: occurance and etiopathology. Indian J Vet Pathol 33:52–57Google Scholar
  50. 50.
    Smits SL, Schapendonk CM, van Leeuwen M, Kuiken T, Bodewes R, Raj VS, Haegmans BL, das Neves CG, Tryland M, Osterhaus AD (2013) Identification and characterization of two novel viruses in ocular infections in reindeer. PloS One 8(7):e69711CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Tamura K, Dudley J, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Tan MT, Yildirim Y, Sozmen M, Bilge Dagalp S, Yilmaz V, Kirmizigul AH, Gokce E (2012) A histopathological, ımmunohistochemical and molecular study of cutaneous bovine papillomatosis. Kafkas Univ Vet Fak Derg 18:739–744Google Scholar
  53. 53.
    Terai M, DeSalle R, Burk RD (2002) Lack of canonical E6 and E7 open reading frames in bird papillomaviruses: Fringilla coelebs papillomavirus and Psittacus erithacus timneh papillomavirus. J Virol 76:10020–10023CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Van Dyk E, Bosman AM, van Wilpe E, Williams JH, Bengis RG, vanHeerden J, Venter EH (2011) Detection and characterisation of papillomavirus in skin lesions of giraffe and sable antelope in South Africa. J S Afr Vet Assoc 82(2):80–85PubMedGoogle Scholar
  55. 55.
    Van Doorslaer Rector A, Vos P, van Ranst M (2006) Genetic characterization of the Capra hircus papillomavirus: A novel close-to-root artiodactyl papillomavirus. Virus Res 118:164–169CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Fırat Dogan
    • 1
  • Selvi Deniz Dorttas
    • 2
  • Seval Bilge Dagalp
    • 2
  • Veysel Soydal Ataseven
    • 1
  • Feray Alkan
    • 2
  1. 1.Faculty of Veterinary Medicine, Department of VirologyMustafa Kemal UniversityHatayTurkey
  2. 2.Faculty of Veterinary Medicine, Department of VirologyAnkara UniversityAnkaraTurkey

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