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Oral HPV prevalence in women positive for cervical HPV infection and their sexual partners: a German screening study

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Abstract

The incidence of human papillomavirus (HPV) associated oropharyngeal squamous cell cancer (OSCC) is on the rise. With the HPV-positive uterine cervix as a reservoir, HPV-positive OSCC is discussed as a sexually transmitted disease. Mechanisms of HPV transmission to the oral cavity are poorly understood. To gain more insight into HPV-transmission routes, cervically HPV-positive women and their sexual partners are screened for oral HPV infection. Women with cervical dysplasia underwent HPV testing of the uterine cervix and tonsillar region via brush test. In addition, sexual partners received oral HPV testing. Tonsillar brush tests of patients admitted for routine surgery served as the control group. The HPV-PCR (Roche Linear Array Kit) was used to differentiate 37 HPV types. All participants completed a risk-factor questionnaire focusing on sexual habits. 101 women were tested HPV-positive at the cervix. Only 3/101 (3 %) were tested HPV-positive in the oropharynx. In 60/101 (60 %) women the sexual partner could be tested for oral HPV infection: testing was positive in 3/60 (5 %). No oral HPV was detected in the control group. The risk-factor questionnaire revealed significant differences between the female study- and control group in terms of age at first sexual intercourse and smoking habits. The limited data suggest that among sexual partners in Germany, HPV transmission to the oropharynx by oral–genital sex or by autoinoculation is a rare and unlikely event with low HPV concordance. Another explanation for the low oral prevalence could be an independent clearance of HPV from the oropharyngeal site compared to cervix uteri or at different time intervals.

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References

  1. Parkin DM, Bray F, Ferlay J, Pisani P (2002) Global cancer statistics. CA Cancer J Clin 55:74–108

    Article  Google Scholar 

  2. Joseph A, Pai S (2011) Human papillomavirus and the shifting trends in head and neck cancer. ASCO:212–6

  3. D’Souza G, Dempsey A (2011) The role of HPV in head and neck cancer and review of the HPV vaccine. Prev Med (Baltim) 53(Suppl 1):S5–S11

    Article  Google Scholar 

  4. Muñoz N, Bosch FX (1992) HPV and cervical neoplasia: review of case–control and cohort studies. IARC Sci Publ:251–61

  5. D’Souza G, Kreimer AR, Viscidi R, Pawlita M, Fakhry C, Koch WM et al (2007) Case–control study of human papillomavirus and oropharyngeal cancer. N Engl J Med 356:1944–1956

    Article  PubMed  Google Scholar 

  6. D’Souza G, Zhang HH, D’Souza WD, Meyer RR, Gillison ML (2010) Moderate predictive value of demographic and behavioral characteristics for a diagnosis of HPV16-positive and HPV16-negative head and neck cancer. Oral Oncol 46:100–104

    Article  PubMed  Google Scholar 

  7. Anantharaman D, Gheit T, Waterboer T, Abedi-Ardekani B, Carreira C, McKay-Chopin S et al (2013) Human papillomavirus infections and upper aero-digestive tract cancers: the ARCAGE study. J Natl Cancer Inst 105:536–545

    Article  CAS  PubMed  Google Scholar 

  8. Smith EM, Ritchie JM, Summersgill KF, Hoffman HT, Wang DH, Haugen TH et al (2004) Human papillomavirus in oral exfoliated cells and risk of head and neck cancer. J Natl Cancer Inst 96:449–455

    Article  PubMed  Google Scholar 

  9. Zhu C, Ling Y, Dong C, Zhou X, Wang F (2012) The relationship between oral squamous cell carcinoma and human papillomavirus: a meta-analysis of a Chinese population (1994–2011). PLoS One 7:e36294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV et al (1999) Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189:12–19

    Article  CAS  PubMed  Google Scholar 

  11. D’Souza G, Agrawal Y, Halpern J, Bodison S, Gillison ML (2009) Oral sexual behaviors associated with prevalent oral human papillomavirus infection. J Infect Dis 199:1263–1269

    Article  PubMed  PubMed Central  Google Scholar 

  12. Gillison ML, Broutian T, Pickard RKL, Tong Z, Xiao W, Kahle L et al (2012) Prevalence of oral HPV infection in the US, 2009–2010. JAMA 307:693–703

    Article  CAS  PubMed  Google Scholar 

  13. Kreimer AR, Alberg AJ, Daniel R, Gravitt PE, Viscidi R, Garrett ES et al (2004) Oral human papillomavirus infection in adults is associated with sexual behavior and HIV serostatus. J Infect Dis 189:686–698

    Article  PubMed  Google Scholar 

  14. Beachler DC, Weber KM, Margolick JB, Strickler HD, Cranston RD, Burk RD et al (2012) Risk factors for oral HPV infection among a high prevalence population of HIV-positive and at-risk HIV-negative adults. Cancer Epidemiol Biomarkers Prev 21:122–133

    Article  CAS  PubMed  Google Scholar 

  15. Smith EM, Ritchie JM, Summersgill KF, Klussmann JP, Lee JH, Wang D et al (2004) Age, sexual behavior and human papillomavirus infection in oral cavity and oropharyngeal cancers. Int J Cancer 108:766–772

    Article  CAS  PubMed  Google Scholar 

  16. Gillison ML, Koch WM, Shah KV (1999) Human papillomavirus in head and neck squamous cell carcinoma: are some head and neck cancers a sexually transmitted disease? Curr Opin Oncol 11:191–199

    Article  CAS  PubMed  Google Scholar 

  17. Pickard RKL, Xiao W, Broutian TR, He X, Gillison ML (2012) The prevalence and incidence of oral human papillomavirus infection among young men and women, aged 18–30 years. Sex Transm Dis 39:559–566

    Article  PubMed  Google Scholar 

  18. Edelstein ZR, Schwartz SM, Hawes S, Hughes JP, Feng Q, Stern ME et al (2012) Rates and determinants of oral human papillomavirus infection in young men. Sex Transm Dis 39:860–867

    Article  PubMed  PubMed Central  Google Scholar 

  19. Widdice LE, Breland DJ, Jonte J, Farhat S, Ma Y, Leonard AC et al (2010) Human papillomavirus concordance in heterosexual couples. J Adolesc Health 47:151–159

    Article  PubMed  PubMed Central  Google Scholar 

  20. zur Hausen H (2000) Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis. J Natl Cancer Inst 92:690–698

    Article  PubMed  Google Scholar 

  21. Dürst M, Glitz D, Schneider A, zur Hausen H (1992) Human papillomavirus type 16 (HPV 16) gene expression and DNA replication in cervical neoplasia: analysis by in situ hybridization. Virology 189:132–140

    Article  PubMed  Google Scholar 

  22. zur Hausen H (1987) Papillomaviruses in human cancer. Appl Pathol 5:19–24

    PubMed  Google Scholar 

  23. Scheurlen W, Stremlau A, Gissmann L, Höhn D, Zenner HP, zur Hausen H (1986) Rearranged HPV 16 molecules in an anal and in a laryngeal carcinoma. Int J Cancer 38:671–676

    Article  CAS  PubMed  Google Scholar 

  24. Löning T, Ikenberg H, Becker J, Gissmann L, Hoepfer I, zur Hausen H (1985) Analysis of oral papillomas, leukoplakias, and invasive carcinomas for human papillomavirus type related DNA. J Invest Dermatol 84:417–420

    Article  PubMed  Google Scholar 

  25. Gillison ML, D’Souza G, Westra W, Sugar E, Xiao W, Begum S et al (2008) Distinct risk factor profiles for human papillomavirus type 16-positive and human papillomavirus type 16-negative head and neck cancers. J Natl Cancer Inst 100:407–420

    Article  PubMed  Google Scholar 

  26. Klussmann JP, Gültekin E, Weissenborn SJ, Wieland U, Dries V, Dienes HP et al (2003) Expression of p16 protein identifies a distinct entity of tonsillar carcinomas associated with human papillomavirus. Am J Pathol 162:747–753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Näsman A, Attner P, Hammarstedt L, Du J, Eriksson M, Giraud G et al (2009) Incidence of human papillomavirus (HPV) positive tonsillar carcinoma in Stockholm, Sweden: an epidemic of viral-induced carcinoma? Int J Cancer 125:362–366

    Article  PubMed  Google Scholar 

  28. Chaturvedi AK, Engels EA, Anderson WF, Gillison ML (2008) Incidence trends for human papillomavirus-related and -unrelated oral squamous cell carcinomas in the US. J Clin Oncol 26:612–619

    Article  PubMed  Google Scholar 

  29. Ndiaye C, Mena M, Alemany L, Arbyn M, Castellsagué X, Laporte L et al (2014) HPV DNA, E6/E7 mRNA, and p16INK4a detection in head and neck cancers: a systematic review and meta-analysis. Lancet Oncol 15:1319–1331

    Article  CAS  PubMed  Google Scholar 

  30. de Lima Rocha MG, Faria FL, Gonçalves L, Souza Mdo CM, Fernandes PÁ, Fernandes AP (2012) Prevalence of DNA-HPV in male sexual partners of HPV-infected women and concordance of viral types in infected couples. PLoS One 7:e40988

    Article  PubMed  Google Scholar 

  31. Fakhry C, D’souza G, Sugar E, Weber K, Goshu E, Minkoff H et al (2006) Relationship between prevalent oral and cervical human papillomavirus infections in human immunodeficiency virus-positive and -negative women. J Clin Microbiol 44:4479–4485

    Article  PubMed  PubMed Central  Google Scholar 

  32. Hernandez BY, Wilkens LR, Zhu X, Thompson P, McDuffie K, Shvetsov YB et al (2008) Transmission of human papillomavirus in heterosexual couples. Emerg Infect Dis 14:888–894

    Article  PubMed  PubMed Central  Google Scholar 

  33. Termine N, Giovannelli L, Matranga D, Perino A, Panzarella V, Ammatuna P et al (2009) Low rate of oral human papillomavirus (HPV) infection in women screened for cervical HPV infection in Southern Italy: a cross-sectional study of 140 immunocompetent subjects. J Med Virol 81:1438–1443

    Article  PubMed  Google Scholar 

  34. Marais DJ, Passmore J-AS, Denny L, Sampson C, Allan BR, Williamson A-L (2008) Cervical and oral human papillomavirus types in HIV-1 positive and negative women with cervical disease in South Africa. J Med Virol 80:953–959

    Article  PubMed  Google Scholar 

  35. Meyer MF, Huebbers CU, Siefer OG, Vent J, Engbert I, Eslick GD et al (2014) Prevalence and risk factors for oral human papillomavirus infection in 129 women screened for cervical HPV infection. Oral Oncol 50:27–31

    Article  PubMed  Google Scholar 

  36. Tristão W, Ribeiro RMP, Oliveira CAD, Betiol JC, Bettini JDSR (2012) Epidemiological study of HPV in oral mucosa through PCR. Braz J Otorhinolaryngol 78:66–70

    Article  PubMed  Google Scholar 

  37. Vidotti LR, Vidal FCB, Monteiro SCM, Nunes JD, Salgado JV, Brito LMO et al (2014) Association between oral DNA-HPV and genital DNA-HPV. J Oral Pathol Med 43:289–292

    Article  PubMed  Google Scholar 

  38. Kellokoski J, Syrjänen S, Yliskoski M, Syrjänen K (1992) Dot blot hybridization in detection of human papillomavirus (HPV) infections in the oral cavity of women with genital HPV infections. Oral Microbiol Immunol 7:19–23

    Article  CAS  PubMed  Google Scholar 

  39. Trottier H, Franco EL (2006) The epidemiology of genital human papillomavirus infection. Vaccine 24(Suppl 1):S1–S15

    PubMed  Google Scholar 

  40. Koutsky PhDL (1997) Epidemiology of genital human papillomavirus infection. Am J Med 102:3–8

    Article  CAS  PubMed  Google Scholar 

  41. Stanley M (2010) Pathology and epidemiology of HPV infection in females. Gynecol Oncol 117:S5–S10

    Article  PubMed  Google Scholar 

  42. Jaisamrarn U, Castellsagué X, Garland SM, Naud P, Palmroth J, Del Rosario-Raymundo MR et al (2013) Natural history of progression of HPV infection to cervical lesion or clearance: analysis of the control arm of the large, randomised PATRICIA study. PLoS One 8:e79260

    Article  PubMed  PubMed Central  Google Scholar 

  43. Vinokurova S, Wentzensen N, Kraus I, Klaes R, Driesch C, Melsheimer P et al (2008) Type-dependent integration frequency of human papillomavirus genomes in cervical lesions. Cancer Res 68:307–313

    Article  CAS  PubMed  Google Scholar 

  44. Liaw KL, Hildesheim A, Burk RD, Gravitt P, Wacholder S, Manos MM et al (2001) A prospective study of human papillomavirus (HPV) type 16 DNA detection by polymerase chain reaction and its association with acquisition and persistence of other HPV types. J Infect Dis 183:8–15

    Article  CAS  PubMed  Google Scholar 

  45. Yamada T, Manos MM, Peto J, Greer CE, Munoz N, Bosch FX et al (1997) Human papillomavirus type 16 sequence variation in cervical cancers: a worldwide perspective. J Virol 71:2463–2472

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Bosch FX, de Sanjosé S (2007) The epidemiology of human papillomavirus infection and cervical cancer. Dis Markers 23:213–227

    Article  PubMed  PubMed Central  Google Scholar 

  47. Termine N, Giovannelli L, Matranga D, Caleca MP, Bellavia C, Perino A et al (2011) Oral human papillomavirus infection in women with cervical HPV infection: new data from an Italian cohort and a metanalysis of the literature. Oral Oncol 47:244–250

    Article  PubMed  Google Scholar 

  48. Smith EM, Ritchie JM, Yankowitz J, Wang D, Turek LP, Haugen TH (2004) HPV prevalence and concordance in the cervix and oral cavity of pregnant women. Infect Dis Obstet Gynecol 12:45–56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. zur Hausen H (2002) Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2:342–350

    Article  PubMed  Google Scholar 

  50. Burd EM (2003) Human papillomavirus and cervical cancer. Clin Microbiol Rev 16:1–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Castellsagué X (2008) Natural history and epidemiology of HPV infection and cervical cancer. Gynecol Oncol 110:S4–S7

    Article  PubMed  Google Scholar 

  52. Baseman JG, Koutsky LA (2005) The epidemiology of human papillomavirus infections. J Clin Virol 32(Suppl 1):S16–S24

    Article  PubMed  Google Scholar 

  53. Franceschi S, Castellsagué X, Dal Maso L, Smith JS, Plummer M, Ngelangel C et al (2002) Prevalence and determinants of human papillomavirus genital infection in men. Br J Cancer 86:705–711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Kero KM, Rautava J, Syrjänen K, Kortekangas-Savolainen O, Grenman S, Syrjänen S (2014) Stable marital relationship protects men from oral and genital HPV infections. Eur J Clin Microbiol Infect Dis 33:1211–1221

    Article  CAS  PubMed  Google Scholar 

  55. Chaturvedi AK, Graubard BI, Pickard RKL, Xiao W, Gillison ML (2014) High-risk oral human papillomavirus load in the US population, National Health and Nutrition Examination Survey 2009–2010. J Infect Dis 210:441–447

    Article  PubMed  PubMed Central  Google Scholar 

  56. Fakhry C, Gillison ML, D’souza G (2014) Tobacco use and oral HPV-16 infection. JAMA 312:14–16

    Article  Google Scholar 

  57. Lawton G, Thomas S, Schonrock J, Monsour F, Frazer I (1992) Human papillomaviruses in normal oral mucosa: a comparison of methods for sample collection. J Oral Pathol Med 21:265–269

    Article  CAS  PubMed  Google Scholar 

  58. García-Closas M, Egan KM, Abruzzo J, Newcomb PA, Titus-Ernstoff L, Franklin T et al (2001) Collection of genomic DNA from adults in epidemiological studies by buccal cytobrush and mouthwash. Cancer Epidemiol Biomarkers Prev 10:687–696

    PubMed  Google Scholar 

  59. Poethko-Müller C, Buttmann-Schweiger N (2014) HPV vaccination coverage in German girls: results of the KiGGS study: first follow-up (KiGGS Wave 1). Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 57:869–877

    Article  PubMed  Google Scholar 

  60. HPV Vaccination Coverage 2014—National HPV Vaccination Program Register. http://www.hpvregister.org.au/research/coverage-data/HPV-Vaccination-Coverage-2014. Accessed 17 Nov 2015

  61. Annual HPV vaccine coverage 2013–2014: by PCT, local authority and area team—Publications—GOV.UK. https://www.gov.uk/government/statistics/annual-hpv-vaccine-coverage-2013-to-2014-by-pct-local-authority-and-area-team. Accessed 21 Nov 2015

  62. Ali H, Guy RJ, Wand H, Read TR, Regan DG, Grulich AE et al (2013) Decline in in-patient treatments of genital warts among young Australians following the national HPV vaccination program. BMC Infect Dis 13:140

    Article  PubMed  PubMed Central  Google Scholar 

  63. Badaracco G, Venuti A, Di Lonardo A, Scambia G, Mozzetti S, Benedetti Panici P et al (1998) Concurrent HPV infection in oral and genital mucosa. J Oral Pathol Med 27:130–134

    Article  CAS  PubMed  Google Scholar 

  64. Castro TMPPG, Bussoloti Filho I, Nascimento VX, Xavier SD (2009) HPV detection in the oral and genital mucosa of women with positive histopathological exam for genital HPV, by means of the PCR. Braz J Otorhinolaryngol 75:167–171

    Article  PubMed  Google Scholar 

  65. Giraldo P, Gonçalves AKS, Pereira SAS, Barros-Mazon S, Gondo ML, Witkin SS (2006) Human papillomavirus in the oral mucosa of women with genital human papillomavirus lesions. Eur J Obstet Gynecol Reprod Biol 126:104–106

    Article  PubMed  Google Scholar 

  66. Richter KL, van Rensburg EJ, van Heerden WFP, Boy SC (2008) Human papilloma virus types in the oral and cervical mucosa of HIV-positive South African women prior to antiretroviral therapy. J Oral Pathol Med 37:555–559

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was funded by the Asklepios Klinik Hamburg GmbH. The authors thank Peter Wohlmuth from the Department of Statistics, ProResearch, Asklepios Klinik Hamburg for helping to analyse the collected data. Special thanks are sent to Jay Moss for proof reading this paper.

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Correspondence to Ingo U. Teudt.

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The authors declare that they have no conflict of interest. Parts of the data were presented at the 30th International Papillomavirus Conference in Lisbon, Portugal 2015.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. However, due to the retrospective type of the study no formal consent was required.

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

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R. B. Uken and I. U. Teudt equally contributed to the article.

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Uken, R.B., Brummer, O., von Schubert-Bayer, C. et al. Oral HPV prevalence in women positive for cervical HPV infection and their sexual partners: a German screening study. Eur Arch Otorhinolaryngol 273, 1933–1942 (2016). https://doi.org/10.1007/s00405-016-3953-1

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  • DOI: https://doi.org/10.1007/s00405-016-3953-1

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