1887

Abstract

Data on cutaneous human papillomavirus (HPV) seroprevalence are primarily derived from skin cancer case–control studies. Few studies have reported the seroprevalence of cutaneous HPV among healthy men. This study investigated the seroprevalence of cutaneous HPV types and associated risk factors among men residing in Brazil, Mexico and the USA. Six hundred men were randomly selected from the HPV Infection in Men study. Archived serum specimens were tested for antibodies against 14 cutaneous HPV genotypes, β-HPV types (5/8/12/14/17/22/23/24/38/48), α-HPV 27, γ-HPV 4, µ-HPV1 and ν-HPV 41 using a glutathione S-transferase L1-based multiplex serology assay. Risk factor data were collected by a questionnaire. Binomial proportions were used to estimate seroprevalence, and logistic regression to examine factors associated with seropositivity. Overall, 65.4 % of men were seropositive to ≥1 of the 14 cutaneous HPV types, and 39.0 % were positive for ≥1 β-HPV types. Seroprevalence was 8.9, 30.9, 28.6 and 9.4 % for α-HPV 27, γ-HPV 4, µ-HPV 1 and ν-HPV 41, respectively. In multivariate analyses, seropositivity for any cutaneous HPV type was associated with higher education [adjusted odds ratio (AOR) 1.75; 95 % confidence interval (CI) 1.08–2.83], and seropositivity of any β-HPV type was significantly associated with increasing age (AOR 1.72; 95 % CI 1.12–2.63, for men aged 31–44 years vs men aged 18–30 years). Other factors associated with various type-specific cutaneous HPV seropositivity included country, circumcision and lifetime number of male sexual partners. These data indicate that exposure to cutaneous HPV is common. Future studies are needed to assess the role of cutaneous HPV in diseases.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000620
2016-12-16
2019-12-08
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/12/3291.html?itemId=/content/journal/jgv/10.1099/jgv.0.000620&mimeType=html&fmt=ahah

References

  1. Albero G., Castellsagué X., Giuliano A. R., Bosch F. X..( 2012;). Male circumcision and genital human papillomavirus: a systematic review and meta-analysis. . Sex Transm Dis 39: 104–113. [CrossRef] [PubMed]
    [Google Scholar]
  2. Albero G., Castellsagué X., Lin H. Y., Fulp W., Villa L. L., Lazcano-Ponce E., Papenfuss M., Abrahamsen M., Salmerón J. et al.( 2014;). Male circumcision and the incidence and clearance of genital human papillomavirus (HPV) infection in men: the HPV Infection in Men (HIM) cohort study. . BMC Infect Dis 14: 75. [CrossRef] [PubMed]
    [Google Scholar]
  3. Andersson K., Waterboer T., Kirnbauer R., Slupetzky K., Iftner T., de Villiers E. M., Forslund O., Pawlita M., Dillner J..( 2008;). Seroreactivity to cutaneous human papillomaviruses among patients with nonmelanoma skin cancer or benign skin lesions. . Cancer Epidemiol Biomarkers Prev 17: 189–195. [CrossRef] [PubMed]
    [Google Scholar]
  4. Antonsson A., Forslund O., Ekberg H., Sterner G., Hansson B. G..( 2000;). The ubiquity and impressive genomic diversity of human skin papillomaviruses suggest a commensalic nature of these viruses. . J Virol 74: 11636–11641.[CrossRef]
    [Google Scholar]
  5. Bernard H. U., Burk R. D., Chen Z., van Doorslaer K., zur Hausen H., de Villiers E. M..( 2010;). Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. . Virology 401: 70–79.[CrossRef]
    [Google Scholar]
  6. Bottalico D., Chen Z., Dunne A., Ostoloza J., McKinney S., Sun C., Schlecht N. F., Fatahzadeh M., Herrero R. et al.( 2011;). The oral cavity contains abundant known and novel human papillomaviruses from the Betapapillomavirus and Gammapapillomavirus genera. . J Infect Dis 204: 787–792. [CrossRef] [PubMed]
    [Google Scholar]
  7. Boxman I. L., Russell A., Mulder L. H., Bavinck J. N., ter Schegget J., Green A.. Collaborators of the Nambour Prevention Study( 2001;). Association between epidermodysplasia verruciformis-associated human papillomavirus DNA in plucked eyebrow hair and solar keratoses. . J Invest Dermatol 117: 1108–1112. [CrossRef] [PubMed]
    [Google Scholar]
  8. Bzhalava D., Guan P., Franceschi S., Dillner J., Clifford G..( 2013;). A systematic review of the prevalence of mucosal and cutaneous human papillomavirus types. . Virology 445: 224–231.[CrossRef]
    [Google Scholar]
  9. Casabonne D., Michael K. M., Waterboer T., Pawlita M., Forslund O., Burk R. D., Travis R. C., Key T. J., Newton R..( 2007;). A prospective pilot study of antibodies against human papillomaviruses and cutaneous squamous cell carcinoma nested in the Oxford component of the European prospective investigation into cancer and nutrition. . Int J Cancer 121: 1862–1868.[CrossRef]
    [Google Scholar]
  10. Chandra A., Mosher W. D., Copen C., Sionean C..( 2011;). Sexual Behavior, Sexual Attraction, and Sexual Identity in the United States: Data from the 2006–2008 National Survey of Family Growth. National Health Statistics Reports, no. 36. Hyattsville, MD:: National Center for Health Statistics;.
    [Google Scholar]
  11. de Koning M. N., Weissenborn S. J., Abeni D., Bouwes Bavinck J. N., Euvrard S., Green A. C., Harwood C. A., Naldi L., Neale R. et al.( 2009;). Prevalence and associated factors of betapapillomavirus infections in individuals without cutaneous squamous cell carcinoma. . J Gen Virol 90: 1611–1621. [CrossRef] [PubMed]
    [Google Scholar]
  12. Dunne E. F., Nielson C. M., Hagensee M. E., Papenfuss M. R., Harris R. B., Herrel N., Gourlie J., Abrahamsen M., Markowitz L. E., Giuliano A. R..( 2009;). HPV 6/11, 16, 18 seroprevalence in men in two US cities. . Sex Transm Dis 36: 671–674. [CrossRef] [PubMed]
    [Google Scholar]
  13. Ekstrom J., Bzhalava D., Svenback D., Forslund O., Dillner J..( 2011;). High throughput sequencing reveals diversity of human papillomaviruses in cutaneous lesions. . Int J Cancer 129: 2643–2650.[CrossRef]
    [Google Scholar]
  14. Farzan S. F., Waterboer T., Gui J., Nelson H. H., Li Z., Michael K. M., Perry A. E., Spencer S. K., Demidenko E. et al.( 2013;). Cutaneous alpha, beta and gamma human papillomaviruses in relation to squamous cell carcinoma of the skin: a population-based study. . Int J Cancer 133: 1713–1720.[CrossRef]
    [Google Scholar]
  15. Feltkamp M. C., Broer R., di Summa F. M., Struijk L., van der Meijden E., Verlaan B. P., Westendorp R. G., ter Schegget J., Spaan W. J., Bavinck J. N. B..( 2003;). Seroreactivity to epidermodysplasia verruciformis-related human papillomavirus types is associated with nonmelanoma skin cancer. . Cancer Res 63: 2695–2700.[PubMed]
    [Google Scholar]
  16. Giuliano A. R., Lazcano-Ponce E., Villa L. L., Flores R., Salmeron J., Lee J.-H., Papenfuss M. R., Abrahamsen M., Jolles E. et al.( 2008;). The human papillomavirus infection in men study: human papillomavirus prevalence and type distribution among men residing in Brazil, Mexico, and the United States. . Cancer Epidemiol Biomarkers Prev 17: 2036–2043. [CrossRef]
    [Google Scholar]
  17. Giuliano A. R., Lazcano E., Villa L. L., Flores R., Salmeron J., Lee J. H., Papenfuss M., Abrahamsen M., Baggio M. L., Silva R..( 2009;). Circumcision and sexual behavior: factors independently associated with human papillomavirus detection among men in the HIM study. . Int J Cancer 124: 1251–1257.[CrossRef]
    [Google Scholar]
  18. Giuliano A. R., Lee J. H., Fulp W., Villa L. L., Lazcano E., Papenfuss M. R., Abrahamsen M., Salmeron J., Anic G. M. et al.( 2011;). Incidence and clearance of genital human papillomavirus infection in men (HIM): a cohort study. . Lancet 377: 932–940.[CrossRef]
    [Google Scholar]
  19. Hampras S. S., Giuliano A. R., Lin H. Y., Fisher K. J., Abrahamsen M. E., Sirak B. A., Iannacone M. R., Gheit T., Tommasino M., Rollison D. E..( 2014;). Natural history of cutaneous human papillomavirus (HPV) infection in men: the HIM study. . PLoS One 9: e104843. [CrossRef] [PubMed]
    [Google Scholar]
  20. Hannigan G. D., Grice E. A..( 2013;). Microbial ecology of the skin in the era of metagenomics and molecular microbiology. . Cold Spring Harb Perspect Med 3: a015362. [CrossRef] [PubMed]
    [Google Scholar]
  21. Hariri S., Dunne E. F., Sternberg M., Unger E. R., Meadows K. S., Karem K. L., Markowitz L. E..( 2008;). Seroepidemiology of human papillomavirus type 11 in the United States: results from the third National Health and Nutrition Examination Survey, 1991–1994. . Sex Transm Dis 35: 298–303.[CrossRef]
    [Google Scholar]
  22. Holm S..( 1979;). A simple sequentially rejective multiple test procedure. . Scand J Stat 6: 65–70.
    [Google Scholar]
  23. Iannacone M. R., Michael K. M., Giuliano A. R., Waterboer T., Pawlita M., Rollison D. E..( 2010;). Risk factors for cutaneous human papillomavirus seroreactivity among patients undergoing skin cancer screening in Florida. . J Infect Dis 201: 760–769. [CrossRef] [PubMed]
    [Google Scholar]
  24. Iannacone M. R., Gheit T., Waterboer T., Giuliano A. R., Messina J. L., Fenske N. A., Cherpelis B. S., Sondak V. K., Roetzheim R. G. et al.( 2012;). Case-control study of cutaneous human papillomaviruses in squamous cell carcinoma of the skin. . Cancer Epidemiol Biomarkers Prev 21: 1303–1313. [CrossRef] [PubMed]
    [Google Scholar]
  25. Karagas M. R., Nelson H. H., Sehr P., Waterboer T., Stukel T. A., Andrew A., Green A. C., Bavinck J. N. B., Perry A., Spencer S..( 2006;). Human papillomavirus infection and incidence of squamous cell and basal cell carcinomas of the skin. . J Natl Cancer Inst 98: 389–395.[CrossRef]
    [Google Scholar]
  26. Karagas M. R., Waterboer T., Li Z., Nelson H. H., Michael K. M., Bavinck J. N., Perry A. E., Spencer S. K., Daling J. et al.( 2010;). Genus beta human papillomaviruses and incidence of basal cell and squamous cell carcinomas of skin: population based case-control study. . BMJ 341: c2986.[CrossRef]
    [Google Scholar]
  27. Kreuter A., Brockmeyer N. H., Weissenborn S. J., Gambichler T., Stucker M., Altmeyer P., Pfister H., Wieland U.. German Competence Network, HIV/AIDS( 2008;). Penile intraepithelial neoplasia is frequent in HIV-positive men with anal dysplasia. . J Invest Dermatol 128: 2316–2324.[CrossRef]
    [Google Scholar]
  28. Lacey C. J., Lowndes C. M., Shah K. V..( 2006;). Burden and management of non-cancerous HPV-related conditions: HPV-6/11 disease. . Vaccine 24: S35–S41. [CrossRef]
    [Google Scholar]
  29. Liu G., Markowitz L. E., Hariri S., Panicker G., Unger E. R..( 2016;). Seroprevalence of 9 human papillomavirus types in the United States 2005-2006. . J Infect Dis 213: 191–198.[CrossRef]
    [Google Scholar]
  30. Lu B., Viscidi R. P., Lee J. H., Wu Y., Villa L. L., Lazcano-Ponce E., da Silva R. J., Baggio M. L., Quiterio M. et al.( 2011;). Human papillomavirus (HPV) 6, 11, 16, and 18 seroprevalence is associated with sexual practice and age: results from the multinational HPV Infection in Men study (HIM study). . Cancer Epidemiol Biomarkers Prev 20: 990–1002. [CrossRef] [PubMed]
    [Google Scholar]
  31. Michael K. M., Waterboer T., Sehr P., Rother A., Reidel U., Boeing H., Bravo I. G., Schlehofer J., Gartner B. C., Pawlita M..( 2008;). Seroprevalence of 34 human papillomavirus types in the German general population. . PLoS Pathog 4: e1000091. [CrossRef] [PubMed]
    [Google Scholar]
  32. Molano M., Posso H., Weiderpass E., van den Brule A. J., Ronderos M., Franceschi S., Meijer C. J., Arslan A., Munoz N., Study H. P. V. S. G. H..( 2002;). Prevalence and determinants of HPV infection among Colombian women with normal cytology. . Br J Cancer 87: 324–333.[CrossRef]
    [Google Scholar]
  33. Parkin D. M., Bray F..( 2006;). The burden of HPV-related cancers. . Vaccine 24: S11–S25. [CrossRef]
    [Google Scholar]
  34. Pierce Campbell C. M., Messina J. L., Stoler M. H., Jukic D. M., Tommasino M., Gheit T., Rollison D. E., Sichero L., Sirak B. A. et al.( 2013;). Cutaneous human papillomavirus types detected on the surface of male external genital lesions: a case series within the HPV Infection in Men study. . J Clin Virol 58: 652–659.[CrossRef]
    [Google Scholar]
  35. Plasmeijer E. I., Struijk L., Bouwes Bavinck J. N., Feltkamp M. C..( 2009;). Epidemiology of cutaneous human papillomavirus infections. . Cancer Treat Res 146: 143–157. [CrossRef] [PubMed]
    [Google Scholar]
  36. Sampogna F., Bavinck J. N., Pawlita M., Abeni D., Harwood C. A., Proby C. M., Feltkamp M. C., Euvrard S., Naldi L. et al.( 2012;). Factors associated with the seroprevalence of 26 cutaneous and two genital human papillomavirus types in organ transplant patients. . J Gen Virol 93: 165–174.[CrossRef]
    [Google Scholar]
  37. Sehr P., Muller M., Hopfl R., Widschwendter A., Pawlita M..( 2002;). HPV antibody detection by ELISA with capsid protein L1 fused to glutathione S-transferase. . J Virol Methods 106: 61–70. [CrossRef] [PubMed]
    [Google Scholar]
  38. Sichero L., Pierce Campbell C. M., Fulp W., Ferreira S., Sobrinho J. S., Baggio M., Galan L., Silva R. C., Lazcano-Ponce E. et al.( 2014;). High genital prevalence of cutaneous human papillomavirus DNA on male genital skin: the HPV Infection in Men study. . BMC Infect Dis 14: 677. [CrossRef] [PubMed]
    [Google Scholar]
  39. Steben M., Garland S. M..( 2014;). Genital warts. . Best Pract Res Clin Obstet Gynaecol 28: 1063–1073. [CrossRef] [PubMed]
    [Google Scholar]
  40. Struijk L., Bouwes Bavinck J. N., Wanningen P., van der Meijden E., Westendorp R. G., ter Schegget J., Feltkamp M. C..( 2003;). Presence of human papillomavirus DNA in plucked eyebrow hairs is associated with a history of cutaneous squamous cell carcinoma. . J Invest Dermatol 121: 1531–1535. [CrossRef] [PubMed]
    [Google Scholar]
  41. Struijk L., Hall L., van der Meijden E., Wanningen P., Bavinck J. N., Neale R., Green A. C., ter Schegget J., Feltkamp M. C..( 2006;). Markers of cutaneous human papillomavirus infection in individuals with tumor-free skin, actinic keratoses, and squamous cell carcinoma. . Cancer Epidemiol Biomarkers Prev 15: 529–535.[CrossRef]
    [Google Scholar]
  42. Svare E. I., Kjaer S. K., Worm A. M., Osterlind A., Meijer C. J., van den Brule A. J..( 2002;). Risk factors for genital HPV DNA in men resemble those found in women: a study of male attendees at a Danish STD clinic. . Sex Transm Infect 78: 215–218. [CrossRef] [PubMed]
    [Google Scholar]
  43. Taylor J. R., Lockwood A. P., Taylor A. J..( 1996;). The prepuce: specialized mucosa of the penis and its loss to circumcision. . Br J Urol 77: 291–295. [CrossRef] [PubMed]
    [Google Scholar]
  44. Tiggelaar S. M., Lin M. J., Viscidi R. P., Ji J., Smith J. S..( 2012;). Age-specific human papillomavirus antibody and deoxyribonucleic acid prevalence: a global review. . J Adolesc Health 50: 110–131. [CrossRef] [PubMed]
    [Google Scholar]
  45. Walboomers J. M., Jacobs M. V, Manos M. M., Bosch F. X, Kummer J. A., Shah K. V, Snijders P. J., Peto J., Meijer C. J., Munoz N..( 1999;). Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. . J Pathol 189: 12–19.[CrossRef]
    [Google Scholar]
  46. Warren J..( 2010;). Physical effects of circumcision. . In Genital Autonomy, pp. 75–79. New York, NY:: Springer;.[CrossRef]
    [Google Scholar]
  47. Waterboer T., Sehr P., Michael K. M., Franceschi S., Nieland J. D., Joos T. O., Templin M. F., Pawlita M..( 2005;). Multiplex human papillomavirus serology based on in situ-purified glutathione S-transferase fusion proteins. . Clin Chem 51: 1845–1853.[CrossRef]
    [Google Scholar]
  48. Waterboer T., Abeni D., Sampogna F., Rother A., Masini C., Sehr P., Michael K. M., Pawlita M..( 2008;). Serological association of beta and gamma human papillomaviruses with squamous cell carcinoma of the skin. . Br J Dermatol 159: 457–459. [CrossRef] [PubMed]
    [Google Scholar]
  49. Wieland U., Jurk S., Weissenborn S., Krieg T., Pfister H., Ritzkowsky A..( 2000;). Erythroplasia of queyrat: coinfection with cutaneous carcinogenic human papillomavirus type 8 and genital papillomaviruses in a carcinoma in situ. . J Invest Dermatol 115: 396–401.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000620
Loading
/content/journal/jgv/10.1099/jgv.0.000620
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error