Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Sexual Health Sexual Health Society
Publishing on sexual health from the widest perspective
RESEARCH ARTICLE

The epidemiology of anal human papillomavirus infection among women and men having sex with women

Alan G. Nyitray
+ Author Affiliations
- Author Affiliations

H. Lee Moffitt Cancer Center and Research Institute, Department of Cancer Epidemiology, 12902 Magnolia Drive, MRC-CANCONT, Tampa, FL 33612, USA. Email: alan.nyitray@moffitt.org

Sexual Health 9(6) 538-546 https://doi.org/10.1071/SH12021
Submitted: 23 February 2012  Accepted: 1 May 2012   Published: 31 August 2012

Abstract

The goal of this review is to summarise epidemiological data that support an understanding of the natural history of anal human papillomavirus (HPV) among women and men having sex with women (MSW). HPV is a common infection of the anal canal among women and MSW. Although there have been a limited number of studies to date, both oncogenic and nononcogenic HPV genotypes commonly occur among these populations even when individuals do not report receptive anal sex. Genotype distribution is quite diverse, with recent studies typically detecting more than two dozen genotypes in the anal canal in samples of women and MSW. Factors most consistently associated with HPV in the anal canal among both women and MSW are lifetime number of sexual partners and detection of HPV at the genitals. The common finding of genotypic concordance between the genitals and anal canal in women and MSW, and the infectious nature of HPV, in addition to a limited number of studies offering empirical evidence of anal-to-genital self-inoculation and evidence of HPV hand carriage, may help explain the detection of HPV in the anal canal outside the context of receptive anal sex. HPV vaccination has been shown to reduce anal HPV infection among women and is also a promising prevention strategy among MSW.

Additional keywords: anal sex, cancer, genital warts, heterosexual, HPV, review.


References

[1]  Piketty C, Darragh TM, Da Costa M, Bruneval P, Heard I, Kazatchkine MD, et al High prevalence of anal human papillomavirus infection and anal cancer precursors among HIV-infected persons in the absence of anal intercourse. Ann Intern Med 2003; 138 453–9.
| 12639077PubMed |

[2]  Wilkin TJ, Palmer S, Brudney KF, Chiasson MA, Wright TC. Anal intraepithelial neoplasia in heterosexual and homosexual HIV-positive men with access to antiretroviral therapy. J Infect Dis 2004; 190 1685–91.
Anal intraepithelial neoplasia in heterosexual and homosexual HIV-positive men with access to antiretroviral therapy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2crgslyrtw%3D%3D&md5=d428b4648c8095f957fff03999327872CAS | 15478076PubMed |

[3]  Park IU, Ogilvie JW, Anderson KE, Li ZZ, Darrah L, Madoff R, et al Anal human papillomavirus infection and abnormal anal cytology in women with genital neoplasia. Gynecol Oncol 2009; 114 399–403.
Anal human papillomavirus infection and abnormal anal cytology in women with genital neoplasia.Crossref | GoogleScholarGoogle Scholar | 19501896PubMed |

[4]  Kojic EM, Cu-Uvin S, Conley L, Bush T, Onyekwuluje J, Swan DC, et al Human papillomavirus infection and cytologic abnormalities of the anus and cervix among HIV-infected women in the Study to Understand the Natural History of HIV/AIDS in the Era of Effective Therapy (The SUN Study). Sex Transm Dis 2011; 38 253–9.
| 20966828PubMed |

[5]  Palefsky JM, Holly EA, Ralston ML, Da Costa M, Greenblatt RM. Prevalence and risk factors for anal human papillomavirus infection in human immunodeficiency virus (HIV)-positive and high-risk HIV-negative women. J Infect Dis 2001; 183 383–91.
Prevalence and risk factors for anal human papillomavirus infection in human immunodeficiency virus (HIV)-positive and high-risk HIV-negative women.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7isFOmuw%3D%3D&md5=60bd6d85587e989686d7e81951a1149aCAS | 11133369PubMed |

[6]  Williams AB, Darragh TM, Vranizan K, Ochia C, Moss AR, Palefsky JM. Anal and cervical human papillomavirus infection and risk of anal and cervical epithelial abnormalities in human immunodeficiency virus-infected women. Obstet Gynecol 1994; 83 205–11.
| 1:STN:280:DyaK2c7hvFCquw%3D%3D&md5=aef334317151c05b3771acaab71975a1CAS | 8290181PubMed |

[7]  Nyitray A, Nielson CM, Harris RB, Flores R, Abrahamsen M, Dunne EF, et al Prevalence of and risk factors for anal human papillomavirus infection in heterosexual men. J Infect Dis 2008; 197 1676–84.
Prevalence of and risk factors for anal human papillomavirus infection in heterosexual men.Crossref | GoogleScholarGoogle Scholar | 18426367PubMed |

[8]  Leung WY, Chan PKS, Lau KH, Ho KM. The prevalence of human papilloma virus in the anal region of male Chinese attendees in three public sexually transmitted disease clinics in Hong Kong. Hong Kong J Dermatol Venereol 2011; 19 6–13.

[9]  Kreimer AR, González P, Katki HA, Porras C, Schiffman M, Rodriguez AC, et al Efficacy of a bivalent HPV 16/18 vaccine against anal HPV 16/18 infection among young women: a nested analysis within the Costa Rica Vaccine Trial. Lancet Oncol 2011; 12 862–70.
Efficacy of a bivalent HPV 16/18 vaccine against anal HPV 16/18 infection among young women: a nested analysis within the Costa Rica Vaccine Trial.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFSqs7%2FF&md5=d553b65b3a0675b65f86fc4eeda27e54CAS | 21865087PubMed |

[10]  Hernandez BY, McDuffie K, Zhu X, Wilkens LR, Killeen J, Kessel B, et al Anal human papillomavirus infection in women and its relationship with cervical infection. Cancer Epidemiol Biomarkers Prev 2005; 14 2550–6.
Anal human papillomavirus infection in women and its relationship with cervical infection.Crossref | GoogleScholarGoogle Scholar | 16284377PubMed |

[11]  Goodman MT, Shvetsov YB, McDuffie K, Wilkens LR, Zhu X, Ning L, et al Acquisition of anal human papillomavirus (HPV) infection in women: the Hawaii HPV Cohort Study. J Infect Dis 2008; 197 957–66.
Acquisition of anal human papillomavirus (HPV) infection in women: the Hawaii HPV Cohort Study.Crossref | GoogleScholarGoogle Scholar | 18429348PubMed |

[12]  Hillemanns P, Ellerbrock TV, McPhillips S, Dole P, Alperstein S, Johnson D, et al Prevalence of anal human papillomavirus infection and anal cytologic abnormalities in HIV-seropositive women. AIDS 1996; 10 1641–7.
| 1:STN:280:DyaK2s7isFKisA%3D%3D&md5=77dba853be5714feeab05a89184937c0CAS | 8970684PubMed |

[13]  Hessol NA, Holly EA, Efird JT, Minkoff H, Schowalter K, Darragh TA, et al Anal intraepithelial neoplasia in a multisite study of HIV-infected and high-risk HIV-uninfected women. AIDS 2009; 23 59–70.
Anal intraepithelial neoplasia in a multisite study of HIV-infected and high-risk HIV-uninfected women.Crossref | GoogleScholarGoogle Scholar | 19050387PubMed |

[14]  Crawford R, Grignon AL, Kitson S, Winder DM, Ball SLR, Vaughan K, et al High prevalence of HPV in non-cervical sites of women with abnormal cervical cytology. BMC Cancer 2011; 11 473
High prevalence of HPV in non-cervical sites of women with abnormal cervical cytology.Crossref | GoogleScholarGoogle Scholar | 22047498PubMed |

[15]  Valari O, Koliopoulos G, Karakitsos P, Valasoulis G, Founta C, Godevenos D, et al Human papillomavirus DNA and mRNA positivity of the anal canal in women with lower genital tract HPV lesions: predictors and clinical implications. Gynecol Oncol. 2011; 122 505–508.
Human papillomavirus DNA and mRNA positivity of the anal canal in women with lower genital tract HPV lesions: predictors and clinical implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvFChu7o%3D&md5=a3757b332bb0980b5caffc6fe4fc3c9fCAS | 21665253PubMed |

[16]  Moscicki AB, Durako SJ, Houser J, Ma Y, Murphy DA, Darragh TM, et al Human papillomavirus infection and abnormal cytology of the anus in HIV-infected and uninfected adolescents. AIDS 2003; 17 311–20.
Human papillomavirus infection and abnormal cytology of the anus in HIV-infected and uninfected adolescents.Crossref | GoogleScholarGoogle Scholar | 12556684PubMed |

[17]  Law CL, Thompson CH, Rose BR, Cossart YE. Anal intercourse: a risk factor for anal papillomavirus infection in women? Genitourin Med 1991; 67 464–8.
| 1:STN:280:DyaK387ivV2itQ%3D%3D&md5=2524456c437ee352dbd50e28af66e33dCAS | 1663485PubMed |

[18]  Palefsky J. Biology of HPV in HIV infection. Adv Dent Res 2006; 19 99–105.
Biology of HPV in HIV infection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283ksl2jtg%3D%3D&md5=9baf730cba54fcd020c2f143bb29bba3CAS | 16672559PubMed |

[19]  Durante AJ, Williams AB, Da Costa M, Darragh TM, Khoshnood K, Palefsky JM. Incidence of anal cytological abnormalities in a cohort of human immunodeficiency virus-infected women. Cancer Epidemiol Biomarkers Prev 2003; 12 638–42.
| 12869403PubMed |

[20]  Conley L, Bush T, Darragh TM, Palefsky JM, Unger ER, Patel P, et al Factors associated with prevalent abnormal anal cytology in a large cohort of HIV-infected adults in the United States. J Infect Dis 2010; 202 1567–76.
Factors associated with prevalent abnormal anal cytology in a large cohort of HIV-infected adults in the United States.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cbhtFOmtw%3D%3D&md5=69e6ad464e4e7e29cf987589aec24e90CAS | 20925532PubMed |

[21]  Tandon R, Baranoski AS, Huang F, de las Morenas A, Vragovic O, Sullivan M, et al Abnormal anal cytology in HIV-infected women. Am J Obstet Gynecol. 2010; 203 21e1–6.
Abnormal anal cytology in HIV-infected women.Crossref | GoogleScholarGoogle Scholar |

[22]  Gonçalves MA, Randi G, Arslan A, Villa LL, Burattini MN, Franceschi S, et al HPV type infection in different anogenital sites among HIV-positive Brazilian women. Infect Agent Cancer 2008; 3 5
HPV type infection in different anogenital sites among HIV-positive Brazilian women.Crossref | GoogleScholarGoogle Scholar | 18341690PubMed |

[23]  Shvetsov YB, Hernandez BY, McDuffie K, Wilkens LR, Zhu XM, Ning L, et al Duration and clearance of anal human papillomavirus (HPV) infection among women: the Hawaii HPV Cohort Study. Clin Infect Dis 2009; 48 536–46.
Duration and clearance of anal human papillomavirus (HPV) infection among women: the Hawaii HPV Cohort Study.Crossref | GoogleScholarGoogle Scholar | 19191636PubMed |

[24]  Goodman MT, Shvetsov YB, McDuffie K, Wilkens LR, Zhu X, Thompson PJ, et al Sequential acquisition of human papillomavirus (HPV) infection of the anus and cervix: the Hawaii HPV Cohort Study. J Infect Dis 2010; 201 1331–9.
Sequential acquisition of human papillomavirus (HPV) infection of the anus and cervix: the Hawaii HPV Cohort Study.Crossref | GoogleScholarGoogle Scholar | 20307204PubMed |

[25]  de Pokomandy A, Rouleau D, Ghattas G, Trottier H, Vezina S, Cote P, et al HAART and progression to high-grade anal intraepithelial neoplasia in men who have sex with men and are infected with HIV. Clin Infect Dis 2011; 52 1174–81.
HAART and progression to high-grade anal intraepithelial neoplasia in men who have sex with men and are infected with HIV.Crossref | GoogleScholarGoogle Scholar | 21364075PubMed |

[26]  Palefsky JM, Holly EA, Ralston ML, Jay N, Berry JM, Darragh TM. High incidence of anal high-grade squamous intra-epithelial lesions among HIV-positive and HIV-negative homosexual and bisexual men. AIDS 1998; 12 495–503.
High incidence of anal high-grade squamous intra-epithelial lesions among HIV-positive and HIV-negative homosexual and bisexual men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3gt1Cmsg%3D%3D&md5=62ca91bfffa2ef7e7e161b4ee1d8ee1cCAS | 9543448PubMed |

[27]  Goodman MT, McDuffie K, Hernandez BY, Wilkens LR, Zhu X, Thompson PJ, et al The influence of multiple human papillomavirus types on the risk of genotype-concordant incident infections of the anus and cervix: the Hawaii HPV Cohort Study. J Infect Dis 2011; 203 335–40.
The influence of multiple human papillomavirus types on the risk of genotype-concordant incident infections of the anus and cervix: the Hawaii HPV Cohort Study.Crossref | GoogleScholarGoogle Scholar | 21208924PubMed |

[28]  Hernandez BY, Wilkens LR, Zhu X, Thompson P, McDuffie K, Shvetsov YB, et al Transmission of human papillomavirus in heterosexual couples. Emerg Infect Dis 2008; 14 888–94.
Transmission of human papillomavirus in heterosexual couples.Crossref | GoogleScholarGoogle Scholar | 18507898PubMed |

[29]  Daling JR, Madeleine MM, Johnson LG, Schwartz SM, Shera KA, Wurscher MA, et al Human papillomavirus, smoking, and sexual practices in the etiology of anal cancer. Cancer 2004; 101 270–80.
Human papillomavirus, smoking, and sexual practices in the etiology of anal cancer.Crossref | GoogleScholarGoogle Scholar | 15241823PubMed |

[30]  Holly EA, Ralston ML, Darragh TM, Greenblatt RM, Jay N, Palefsky JM. Prevalence and risk factors for anal squamous intraepithelial lesions in women. J Natl Cancer Inst 2001; 93 843–9.
Prevalence and risk factors for anal squamous intraepithelial lesions in women.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MzltVCmtg%3D%3D&md5=f7949983d40310348e70bcb60710100fCAS | 11390533PubMed |

[31]  Nyitray AG, Carvalho da Silva RJ, Baggio ML, Lu B, Smith D, Abrahamsen M, et al Age-specific prevalence of and risk factors for anal human papillomavirus (HPV) among men who have sex with women and men who have sex with men: the HPV In Men (HIM) Study. J Infect Dis 2011; 203 49–57.
Age-specific prevalence of and risk factors for anal human papillomavirus (HPV) among men who have sex with women and men who have sex with men: the HPV In Men (HIM) Study.Crossref | GoogleScholarGoogle Scholar | 21148496PubMed |

[32]  Burchell AN, Richardson H, Mahmud SM, Trottier H, Tellier PP, Hanley J, et al Modeling the sexual transmissibility of human papillomavirus infection using stochastic computer simulation and empirical data from a cohort study of young women in Montreal, Canada. Am J Epidemiol 2006; 163 534–43.
Modeling the sexual transmissibility of human papillomavirus infection using stochastic computer simulation and empirical data from a cohort study of young women in Montreal, Canada.Crossref | GoogleScholarGoogle Scholar | 16421235PubMed |

[33]  Partridge JM, Hughes JP, Feng Q, Winer RL, Weaver BA, Xi LF, et al Genital human papillomavirus infection in men: incidence and risk factors in a cohort of university students. J Infect Dis 2007; 196 1128–36.
Genital human papillomavirus infection in men: incidence and risk factors in a cohort of university students.Crossref | GoogleScholarGoogle Scholar | 17955430PubMed |

[34]  Sonnex C, Strauss S, Gray JJ. Detection of human papillomavirus DNA on the fingers of patients with genital warts. Sex Transm Infect 1999; 75 317–9.
Detection of human papillomavirus DNA on the fingers of patients with genital warts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2FotlOhug%3D%3D&md5=02d5fb40c27c883b8f3fbfe7d496e504CAS | 10616355PubMed |

[35]  Moscicki AB, Hills NK, Shiboski S, Darragh TM, Jay N, Powell K, et al Risk factors for abnormal anal cytology in young heterosexual women. Cancer Epidemiol Biomarkers Prev 1999; 8 173–8.
| 1:STN:280:DyaK1M7msFWguw%3D%3D&md5=a479c9ae12d39b68bb6602d02e2ff07aCAS | 10067816PubMed |

[36]  Shvetsov YB, Hernandez BY, Wilkens LR, Thompson PJ, Franke AA, Zhu XM, et al Plasma micronutrients and the acquisition and clearance of anal human papillomavirus infection: the Hawaii HPV Cohort Study. Cancer Res 2010; 70 9787–97.
Plasma micronutrients and the acquisition and clearance of anal human papillomavirus infection: the Hawaii HPV Cohort Study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFamurvI&md5=5522960366ee16f18c996b53657a4dcbCAS | 20935226PubMed |

[37]  Nicolau SM, Camargo CG, Stavale JN, Castelo A, Dores GB, Lorincz A, et al Human papillomavirus DNA detection in male sexual partners of women with genital human papillomavirus infection. Urology 2005; 65 251–5.
Human papillomavirus DNA detection in male sexual partners of women with genital human papillomavirus infection.Crossref | GoogleScholarGoogle Scholar | 15708032PubMed |

[38]  Van Doornum GJ, Prins M, Juffermans LH, Hooykaas C, van den Hoek JA, Coutinho RA, et al Regional distribution and incidence of human papillomavirus infections among heterosexual men and women with multiple sexual partners: a prospective study. Genitourinary Medicine 1994; 70 240–6.
| 1:STN:280:DyaK2M%2FkvVejtQ%3D%3D&md5=f0fac94932dfb27882f7d9ab5fdf5761CAS | 7959707PubMed |

[39]  Nyitray AG, Smith D, Villa L, Lazcano-Ponce E, Abrahamsen M, Papenfuss M, et al Prevalence of and risk factors for anal human papillomavirus infection in men who have sex with women: a cross-national study. J Infect Dis 2010; 201 1498–508.
Prevalence of and risk factors for anal human papillomavirus infection in men who have sex with women: a cross-national study.Crossref | GoogleScholarGoogle Scholar | 20367457PubMed |

[40]  Yu CT, Chao SC, Lee HC, Chou CY, Ko WC, Liu HY, et al High prevalence of anal human papillomavirus infection and associated risky behaviors in men infected with human immunodeficiency virus in Taiwan. AIDS Behav 2012;
High prevalence of anal human papillomavirus infection and associated risky behaviors in men infected with human immunodeficiency virus in Taiwan.Crossref | GoogleScholarGoogle Scholar |

[41]  Sirera G, Videla S, Pinol M, Canadas MP, Llatjos M, Ballesteros AL, et al High prevalence of human papillomavirus infection in the anus, penis and mouth in HIV-positive men. AIDS 2006; 20 1201–4.
High prevalence of human papillomavirus infection in the anus, penis and mouth in HIV-positive men.Crossref | GoogleScholarGoogle Scholar | 16691074PubMed |

[42]  Nyitray AG, Carvalho da Silva RJ, Baggio ML, Smith D, Abrahamsen M, Papenfuss M, et al Six-month incidence, persistence, and factors associated with persistence of anal human papillomavirus in men: the HPV In Men Study. J Infect Dis 2011; 204 1711–22.
Six-month incidence, persistence, and factors associated with persistence of anal human papillomavirus in men: the HPV In Men Study.Crossref | GoogleScholarGoogle Scholar | 21964400PubMed |

[43]  Chaturvedi AK. Beyond cervical cancer: burden of other HPV-related cancers among men and women. J Adolesc Health 2010; 46 S20–6.
Beyond cervical cancer: burden of other HPV-related cancers among men and women.Crossref | GoogleScholarGoogle Scholar | 20307840PubMed |

[44]  Giuliano AR, Lazcano E, Villa LL, Flores R, Salmeron J, Lee JH, et al Circumcision and sexual behavior: factors independently associated with human papillomavirus detection among men in the HIM study. Int J Cancer 2009; 124 1251–7.
Circumcision and sexual behavior: factors independently associated with human papillomavirus detection among men in the HIM study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFGhu7c%3D&md5=09fe540a6606e1ab0cfcfb8333711be2CAS | 19089913PubMed |

[45]  Franceschi S, Castellsague X, Dal Maso L, Smith JS, Plummer M, Ngelangel C, et al Prevalence and determinants of human papillomavirus genital infection in men. Br J Cancer 2002; 86 705–11.
Prevalence and determinants of human papillomavirus genital infection in men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387jvVygtA%3D%3D&md5=e806434cca6de59f9d2c664ed6e5ad70CAS | 11875730PubMed |

[46]  Vaccarella S, Lazcano-Ponce E, Castro-Garduno JA, Cruz-Valdez A, Diaz V, Schiavon R, et al Prevalence and determinants of human papillomavirus infection in men attending vasectomy clinics in Mexico. Int J Cancer 2006; 119 1934–9.
Prevalence and determinants of human papillomavirus infection in men attending vasectomy clinics in Mexico.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1Snsbs%3D&md5=1f074e994896e0241081bb2ea744f09bCAS | 16708372PubMed |

[47]  Ferenczy A, Bergeron C, Richart RM. Human papillomavirus DNA in fomites on objects used for the management of patients with genital human papillomavirus infections. Obstet Gynecol 1989; 74 950–4.
| 1:STN:280:DyaK3c%2Fmslelug%3D%3D&md5=da4bb2c7f2d8b2c38bc194d74cf5c497CAS | 2555753PubMed |

[48]  Palefsky JM, Giuliano AR, Goldstone S, Moreira ED, Aranda C, Jessen H, et al HPV vaccine against anal HPV infection and anal intraepithelial neoplasia. N Engl J Med 2011; 365 1576–85.
HPV vaccine against anal HPV infection and anal intraepithelial neoplasia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVSrsrbN&md5=5aa2abd713524740622154793fcda290CAS | 22029979PubMed |

[49]  Giuliano AR, Lee JH, Fulp W, Villa LL, Lazcano E, Papenfuss MR, et al Incidence and clearance of genital human papillomavirus infection in men (HIM): a cohort study. Lancet 2011; 377 932–40.
Incidence and clearance of genital human papillomavirus infection in men (HIM): a cohort study.Crossref | GoogleScholarGoogle Scholar | 21367446PubMed |

[50]  Roka S, Rasoul-Rockenschaub S, Roka J, Kirnbauer R, Muhlbacher F, Salat A. Prevalence of anal HPV infection in solid-organ transplant patients prior to immunosuppression. Transpl Int 2004; 17 366–9.
Prevalence of anal HPV infection in solid-organ transplant patients prior to immunosuppression.Crossref | GoogleScholarGoogle Scholar | 15349721PubMed |

[51]  Ogunbiyi OA, Scholefield JH, Raftery AT, Smith JH, Duffy S, Sharp F, et al Prevalence of anal human papillomavirus infection and intraepithelial neoplasia in renal allograft recipients. Br J Surg 1994; 81 365–7.
Prevalence of anal human papillomavirus infection and intraepithelial neoplasia in renal allograft recipients.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c3ivVantQ%3D%3D&md5=812f21b705fa5ba26f711dbbb3d7e26aCAS | 8173899PubMed |

[52]  Donovan B, Franklin N, Guy R, Grulich AE, Regan DG, Ali H, et al Quadrivalent human papillomavirus vaccination and trends in genital warts in Australia: analysis of national sentinel surveillance data. Lancet Infect Dis 2011; 11 39–44.
Quadrivalent human papillomavirus vaccination and trends in genital warts in Australia: analysis of national sentinel surveillance data.Crossref | GoogleScholarGoogle Scholar | 21067976PubMed |