World Journal of Urology

, Volume 32, Issue 5, pp 1199–1204 | Cite as

Is real-time PCR the correct method to evaluate the incidence of human papillomavirus in prepuces of asymptomatic boys and men?

  • Isabel Heidegger
  • Renate Pichler
  • Barbara Müller
  • Helmut Klocker
  • David Oswald
  • Bernhard Haid
  • Bettina Zelger
  • Wolfgang Horninger
  • Josef Oswald
Original Article

Abstract

Objective

To investigate the prevalence of human papillomavirus (HPV) in prepuces of asymptomatic boys and men, the present study was designed.

Methods

Two hundred and fifty male prepuce specimens who underwent circumcision due to phimosis were collected. Samples were subdivided into groups regarding their age: children (group I, 0–10 years), adolescents (group II, 11–20 years) and adults (group III, >20 years). HPV High Screen Real-TM Quant 2x kit detecting HPV 6 and 11 (low risk) as well as another kit for identification of HPV 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58 and 59 (high risk) were used. Additionally, a Taq Man assay has been designed targeting the L1 gene of HPV 6, 11, 16 and 18.

Results

Evaluating the number of low-risk HPV subtypes, we found HPV 6 and 11 in 5.3 % of samples (n = 12/226). Concerning high-risk HPV, we found a positivity in 4 % of samples (n = 9/224). In contrast to low-risk data where no age distribution was observed, we found an age-specific accumulation of high-risk HPV subtypes in the children group (n = 6/9). A second independent assay (Taq Man PCR assay) measuring HPV 6, 11, 16 and 18 of all positive samples confirmed only the high-risk HPV subtypes of the Real-TM Quant 2x assay.

Conclusions

Our study provides evidence that qPCR estimation for HPV infection obviously underestimates the incidence rate of infected prepuces in boys and men with phimosis. Contrary, an overestimation of the HPV infection rate with the in situ hybridization method of phimotic prepuces cannot be excluded.

Keywords

Low-risk HPV High-risk HPV Prepuce Phimosis Real-time PCR 

Abbreviations

HPV

Human papilloma virus

DNA

Deribonuclein acid

ISH

In situ hybridization

qPCR

Real-time polymerase change reaction

Notes

Acknowledgments

We thank Dr. Elisabeth Tafatsch for helping with qPCR.

Conflict of interest

Authors have no conflict of interest regarding this article.

References

  1. 1.
    Horvath CA, Boulet GA, Renoux VM, Delvenne PO, Bogers JP (2010) Mechanisms of cell entry by human papillomaviruses: an overview. Virol J 7:11PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Lacey CJ, Lowndes CM, Shah KV (2006) Chapter 4: burden and management of non-cancerous HPV-related conditions: HPV-6/11 disease. Vaccine 24(Suppl 3):S3-35–S3-41Google Scholar
  3. 3.
    Moscicki AB, Schiffman M, Kjaer S, Villa LL (2006) Chapter 5: updating the natural history of HPV and anogenital cancer. Vaccine 24(Suppl 3):S3-42–S3-51Google Scholar
  4. 4.
    Cuzick J, Arbyn M, Sankaranarayanan R, Tsu V, Ronco G, Mayrand MH et al (2008) Overview of human papillomavirus-based and other novel options for cervical cancer screening in developed and developing countries. Vaccine 26(Suppl 10):K29–K41PubMedCrossRefGoogle Scholar
  5. 5.
    Pow-Sang MR, Ferreira U, Pow-Sang JM, Nardi AC, Destefano V (2010) Epidemiology and natural history of penile cancer. Urology 76(2 Suppl 1):S2–S6PubMedCrossRefGoogle Scholar
  6. 6.
    Kjaer SK, Munk C, Winther JF, Jorgensen HO, Meijer CJ, van den Brule AJ (2005) Acquisition and persistence of human papillomavirus infection in younger men: a prospective follow-up study among Danish soldiers. Cancer Epidemiol Biomarkers Prev 14(6):1528–1533PubMedCrossRefGoogle Scholar
  7. 7.
    Partridge JM, Hughes JP, Feng Q, Winer RL, Weaver BA, Xi LF et al (2007) Genital human papillomavirus infection in men: incidence and risk factors in a cohort of university students. J Infect Dis 196(8):1128–1136PubMedCrossRefGoogle Scholar
  8. 8.
    Pilatz A, Altinkilic B, Rusz A, Izykowski N, Traenkenschuh W, Rische J et al (2013) Role of human papillomaviruses in persistent and glucocorticoid-resistant juvenile phimosis. J Eur Acad Dermatol Venereol 27(6):716–721 Google Scholar
  9. 9.
    de Martino M, Haitel A, Wrba F, Schatzl G, Klatte T, Waldert M (2013) High-risk human papilloma virus infection of the foreskin in asymptomatic boys. Urology 81(4):869–872 PubMedCrossRefGoogle Scholar
  10. 10.
    Verit A, Zeyrek FY, Mordeniz C, Ciftci H, Savas M (2012) Status of high-risk oncogenic human papillomavirus subtypes harbored in the prepuce of prepubertal boys. Urology 80(2):423–426PubMedCrossRefGoogle Scholar
  11. 11.
    Canadas MP, Darwich L, Videla S, Sirera G, Coll J, Rafael ML et al (2013) Circumcision and penile human papillomavirus prevalence in human immunodeficiency virus-infected men: heterosexual and men who have sex with men. Clin Microbiol Infect 19(7):611–616Google Scholar
  12. 12.
    Backes DM, Snijders PJ, Hudgens MG, Bailey RC, Bogaarts M, Agot K et al (2013) Sexual behaviour and less frequent bathing are associated with higher human papillomavirus incidence in a cohort study of uncircumcised Kenyan men. Sex Transm Infect 89(2):148–155PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Castellsague X, Bosch FX, Munoz N, Meijer CJ, Shah KV, de Sanjose S et al (2002) Male circumcision, penile human papillomavirus infection, and cervical cancer in female partners. N Engl J Med 346(15):1105–1112PubMedCrossRefGoogle Scholar
  14. 14.
    Vanbuskirk K, Winer RL, Hughes JP, Feng Q, Arima Y, Lee SK et al (2011) Circumcision and acquisition of human papillomavirus infection in young men. Sex Transm Dis 38(11):1074–1081PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Heidegger I, Ofer P, Doppler W, Rotter V, Klocker H, Massoner P (2012) Diverse functions of IGF/insulin signaling in malignant and noncancerous prostate cells: proliferation in cancer cells and differentiation in noncancerous cells. Endocrinology 153(10):4633–4643PubMedCrossRefGoogle Scholar
  16. 16.
    Massoner P, Ladurner RM, Heidegger I, Kloss-Brandstatter A, Summerer M, Reichhart E et al (2011) Expression of the IGF axis is decreased in local prostate cancer but enhanced after benign prostate epithelial differentiation and TGF-β treatment. Am J Pathol 179(6):2905–2919PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Klinglmair G, Pichler R, Zelger B, Dogan HS, Becker T, Esterbauer J et al (2012) Prevalence of the human papillomavirus (HPV) expression of the inner prepuce in asymptomatic boys and men. World J Urol. doi: 10.1007/s00345-012-0997-8
  18. 18.
    Agarwal SS, Sehgal A, Sardana S, Kumar A, Luthra UK (1993) Role of male behavior in cervical carcinogenesis among women with one lifetime sexual partner. Cancer 72(5):1666–1669PubMedCrossRefGoogle Scholar
  19. 19.
    Larke N, Thomas SL, Dos SSI, Weiss HA (2011) Male circumcision and human papillomavirus infection in men: a systematic review and meta-analysis. J Infect Dis 204(9):1375–1390PubMedCrossRefGoogle Scholar
  20. 20.
    Mammas IN, Sourvinos G, Spandidos DA (2009) Human papilloma virus (HPV) infection in children and adolescents. Eur J Pediatr 168(3):267–273PubMedCrossRefGoogle Scholar
  21. 21.
    Doerfler D, Bernhaus A, Kottmel A, Sam C, Koelle D, Joura EA (2009) Human papilloma virus infection prior to coitarche. Am J Obstet Gynecol 200(5):487.e1–487.e5 CrossRefGoogle Scholar
  22. 22.
    Baay MF, Quint WG, Koudstaal J, Hollema H, Duk JM, Burger MP et al (1996) Comprehensive study of several general and type-specific primer pairs for detection of human papillomavirus DNA by PCR in paraffin-embedded cervical carcinomas. J Clin Microbiol 34(3):745–747PubMedPubMedCentralGoogle Scholar
  23. 23.
    Lin MH, Chen TC, Kuo TT, Tseng CC, Tseng CP (2000) Real-time PCR for quantitative detection of Toxoplasma gondii. J Clin Microbiol 38(11):4121–4125PubMedPubMedCentralGoogle Scholar
  24. 24.
    Clementi M (2000) Quantitative molecular analysis of virus expression and replication. J Clin Microbiol 38(6):2030–2036PubMedPubMedCentralGoogle Scholar
  25. 25.
    Biedermann K, Dandachi N, Trattner M, Vogl G, Doppelmayr H, More E et al (2004) Comparison of real-time PCR signal-amplified in situ hybridization and conventional PCR for detection and quantification of human papillomavirus in archival cervical cancer tissue. J Clin Microbiol 42(8):3758–3765PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Kelesidis T, Aish L, Steller MA, Aish IS, Shen J, Foukas P et al (2011) Human papillomavirus (HPV) detection using in situ hybridization in histologic samples: correlations with cytologic changes and polymerase chain reaction HPV detection. Am J Clin Pathol 136(1):119–127PubMedCrossRefGoogle Scholar
  27. 27.
    Dabic MM, Hlupic L, Babic D, Jukic S, Seiwerth S (2004) Comparison of polymerase chain reaction and catalyzed signal amplification in situ hybridization methods for human papillomavirus detection in paraffin-embedded cervical preneoplastic and neoplastic lesions. Arch Med Res 35(6):511–516PubMedCrossRefGoogle Scholar
  28. 28.
    Unger ER, Vernon SD, Lee DR, Miller DL, Reeves WC (1998) Detection of human papillomavirus in archival tissues. Comparison of in situ hybridization and polymerase chain reaction. J Histochem Cytochem 46(4):535–540PubMedCrossRefGoogle Scholar
  29. 29.
    Guo M, Gong Y, Deavers M, Silva EG, Jan YJ, Cogdell DE et al (2008) Evaluation of a commercialized in situ hybridization assay for detecting human papillomavirus DNA in tissue specimens from patients with cervical intraepithelial neoplasia and cervical carcinoma. J Clin Microbiol 46(1):274–280PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Abreu AL, Souza RP, Gimenes F, Consolaro ME (2012) A review of methods for detect human Papillomavirus infection. Virol J 9:262PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Isabel Heidegger
    • 3
  • Renate Pichler
    • 3
  • Barbara Müller
    • 3
  • Helmut Klocker
    • 3
  • David Oswald
    • 2
  • Bernhard Haid
    • 1
  • Bettina Zelger
    • 3
  • Wolfgang Horninger
    • 3
  • Josef Oswald
    • 1
    • 3
  1. 1.Department of Paediatric UrologyHospital St VinzenzLinzAustria
  2. 2.Medical University of SalzburgSalzburgAustria
  3. 3.Department of UrologyMedical University of InnsbruckLinzAustria

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