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RESEARCH ARTICLE

The epidemiology and natural history of anal human papillomavirus infection in men who have sex with men

Dorothy A. Machalek A , Andrew E. Grulich A , Fengyi Jin A , David J. Templeton A B and I. Mary Poynten A C
+ Author Affliations
- Author Affliations

A The Kirby Institute for Infection and Immunity in Society, The University of New South Wales, Sydney, NSW 2052, Australia.

B Royal Prince Alfred Sexual Health, Royal Prince Alfred Hospital, Sydney, NSW 2050, Australia.

C Corresponding author. Email: mpoynten@kirby.unsw.edu.au

Sexual Health 9(6) 527-537 https://doi.org/10.1071/SH12043
Submitted: 2 April 2012  Accepted: 30 July 2012   Published: 27 November 2012

Abstract

Studies on the epidemiology and natural history of anal human papillomavirus (HPV) infection are essential to understand the significance of this virus in the aetiology of anal cancer in men who have sex with men (MSM). This paper presents a review of studies on anal HPV in MSM. For this review, a Medline search was performed to identify English-language articles published in peer-reviewed journals on the epidemiology, natural history and risk factors for anal HPV infection in MSM. Anal HPV prevalence is high in MSM and infection with multiple HPV types is common. The available prospective data suggest detection of new anal HPV infections may also be common. However, with limited epidemiological data available on infection dynamics and associated behavioural risk factors, it is difficult to draw conclusions on how persistent anal HPV infection is in this population.

Additional keywords: anal intraepithelial neoplasia, cancer, homosexual.


References

[1]  Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, et al A review of human carcinogens – part B: biological agents. Lancet Oncol 2009; 10 321–2.
A review of human carcinogens – part B: biological agents.CrossRef | open url image1

[2]  Trottier H, Mahmud SM, Lindsay L, Jenkins D, Quint W, Wieting SL, et al Persistence of an incident human papillomavirus infection and timing of cervical lesions in previously unexposed young women. Cancer Epidemiol Biomarkers Prev 2009; 18 854–62.
Persistence of an incident human papillomavirus infection and timing of cervical lesions in previously unexposed young women.CrossRef | 1:CAS:528:DC%2BD1MXivVOlsb4%3D&md5=f9a072aac5bbb33ecdb41250b8fcc7c4CAS | open url image1

[3]  zur Hausen H. Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis. J Natl Cancer Inst 2000; 92 690–8.
Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis.CrossRef | 1:CAS:528:DC%2BD3cXjslSns7Y%3D&md5=efbdc730ffd4c9019cb699b29ce9f917CAS | open url image1

[4]  Grulich AE, Jin F, Conway EL, Stein AN, Hocking J. Cancers attributable to human papillomavirus infection. Sex Health 2010; 7 244–52.
Cancers attributable to human papillomavirus infection.CrossRef | open url image1

[5]  Jin F, Stein AN, Conway EL, Regan DG, Law M, Brotherton JM, et al Trends in anal cancer in Australia, 1982–2005. Vaccine 2011; 29 2322–7.
Trends in anal cancer in Australia, 1982–2005.CrossRef | open url image1

[6]  Joseph DA, Miller JW, Wu X, Chen VW, Morris CR, Goodman MT, et al Understanding the burden of human papillomavirus-associated anal cancers in the US. Cancer 2008; 113 2892–900.
Understanding the burden of human papillomavirus-associated anal cancers in the US.CrossRef | open url image1

[7]  Frisch M. On the etiology of anal squamous carcinoma. Dan Med Bull 2002; 49 194–209. open url image1

[8]  D’Souza G, Wiley DJ, Li X, Chmiel JS, Margolick JB, Cranston RD, et al Incidence and epidemiology of anal cancer in the multicenter AIDS cohort study. J Acquir Immune Defic Syndr 2008; 48 491–9.
Incidence and epidemiology of anal cancer in the multicenter AIDS cohort study.CrossRef | open url image1

[9]  Machalek DA, Poynten M, Jin F, Fairley CK, Farnsworth A, Garland SM, et al Anal human papillomavirus infection and associated neoplastic lesions in men who have sex with men: a systematic review and meta-analysis. Lancet Oncol 2012; 13 487–500.
Anal human papillomavirus infection and associated neoplastic lesions in men who have sex with men: a systematic review and meta-analysis.CrossRef | open url image1

[10]  Daling JR, Weiss NS, Hislop TG, Maden C, Coates RJ, Sherman KJ, et al Sexual practices, sexually transmitted diseases, and the incidence of anal cancer. N Engl J Med 1987; 317 973–7.
Sexual practices, sexually transmitted diseases, and the incidence of anal cancer.CrossRef | 1:STN:280:DyaL1c%2FhsVSgtg%3D%3D&md5=651553935aeed99ac143a7b52879ed1bCAS | open url image1

[11]  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 | open url image1

[12]  Silverberg MJ, Lau B, Justice AC, Engels E, Gill MJ, Goedert JJ, et al Risk of anal cancer in HIV-infected and HIV-uninfected individuals in North America. Clin Infect Dis 2012; 54 270–80.
Risk of anal cancer in HIV-infected and HIV-uninfected individuals in North America.CrossRef | open url image1

[13]  Gervaz P, Hirschel B, Morel P. Molecular biology of squamous cell carcinoma of the anus. Br J Surg 2006; 93 531–8.
Molecular biology of squamous cell carcinoma of the anus.CrossRef | 1:STN:280:DC%2BD283gvFChug%3D%3D&md5=b3c44fef21ab8fac2c232168b1c54ecdCAS | open url image1

[14]  Watson AJ, Smith BB, Whitehead MR, Sykes PH, Frizelle FA. Malignant progression of anal intra-epithelial neoplasia. ANZ J Surg 2006; 76 715–7.
Malignant progression of anal intra-epithelial neoplasia.CrossRef | open url image1

[15]  Bernard HU, Burk RD, Chen Z, van Doorslaer K, Hausen H, de Villiers EM. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 2010; 401 70–9.
Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments.CrossRef | 1:CAS:528:DC%2BC3cXksVaktbs%3D&md5=d7b4474e14bd195d1ad6dd684100c731CAS | open url image1

[16]  Schiffman M, Herrero R, Desalle R, Hildesheim A, Wacholder S, Rodriguez AC, et al The carcinogenicity of human papillomavirus types reflects viral evolution. Virology 2005; 337 76–84.
The carcinogenicity of human papillomavirus types reflects viral evolution.CrossRef | 1:CAS:528:DC%2BD2MXks1Cru70%3D&md5=29af62959832396a4a2f6110633ef329CAS | open url image1

[17]  Bosch FX, Burchell AN, Schiffman M, Giuliano AR, de Sanjose S, Bruni L, et al Epidemiology and natural history of human papillomavirus infections and type-specific implications in cervical neoplasia. Vaccine 2008; 26 K1–16.
Epidemiology and natural history of human papillomavirus infections and type-specific implications in cervical neoplasia.CrossRef | open url image1

[18]  Lacey CJ, Lowndes CM, Shah KV. Chapter 4: burden and management of non-cancerous HPV-related conditions: HPV-6/11 disease. Vaccine 2006; 24 35–41. open url image1

[19]  Doorbar J, Raj K. Biology of papillomavirus replication in infected epthelium. Future Virol 2007; 2 573–86.
| 1:CAS:528:DC%2BD2sXht1erurnM&md5=7441dd34a3f53a1ea048e77095111774CAS | open url image1

[20]  Herfs M, Hubert P, Moutschen M, Delvenne P. Mucosal junctions: open doors to HPV and HIV infections? Trends Microbiol 2011; 19 114–20.
Mucosal junctions: open doors to HPV and HIV infections?CrossRef | 1:CAS:528:DC%2BC3MXjsFGis7o%3D&md5=edb63c577303b7f0db13c89f4a050baeCAS | open url image1

[21]  Jay N, Berry JM, Hogeboom CJ, Holly EA, Darragh TM, Palefsky JM. Colposcopic appearance of anal squamous intraepithelial lesions: relationship to histopathology. Dis Colon Rectum 1997; 40 919–28.
Colposcopic appearance of anal squamous intraepithelial lesions: relationship to histopathology.CrossRef | 1:STN:280:DyaK2svhtleqsQ%3D%3D&md5=a7f196a8d95e3cf95bca0dd45df9185cCAS | open url image1

[22]  Mukonoweshuro P, Oriowolo A, Smith M. Audit of the histological definition of cervical transformation zone. J Clin Pathol 2005; 58 671
| 1:STN:280:DC%2BD2M3nsVCqtg%3D%3D&md5=0ee6ba52ab356dbbc3ce5ce1b55b16b7CAS | open url image1

[23]  Northfelt DW, Swift PS, Palefsky JM. Anal neoplasia. Pathogenesis, diagnosis, and management. Hematol Oncol Clin North Am 1996; 10 1177–87.
Anal neoplasia. Pathogenesis, diagnosis, and management.CrossRef | 1:STN:280:DyaK2s%2FjsVGnug%3D%3D&md5=0f2da0a17d389ab4e328ff6a5de92a77CAS | open url image1

[24]  Ostör AG. Natural history of cervical intraepithelial neoplasia: a critical review. Int J Gynecol Pathol 1993; 12 186–92.
Natural history of cervical intraepithelial neoplasia: a critical review.CrossRef | open url image1

[25]  Stoler MH, Schiffman M. Interobserver reproducibility of cervical cytologic and histologic interpretations: realistic estimates from the ASCUS-LSIL Triage Study. JAMA 2001; 285 1500–5.
Interobserver reproducibility of cervical cytologic and histologic interpretations: realistic estimates from the ASCUS-LSIL Triage Study.CrossRef | 1:STN:280:DC%2BD3M7osFClsg%3D%3D&md5=d9b6a0e345f70408c870c46e8d2dd24fCAS | open url image1

[26]  Agorastos T, Miliaras D, Lambropoulos AF, Chrisafi S, Kotsis A, Manthos A, et al Detection and typing of human papillomavirus DNA in uterine cervices with coexistent grade I and grade III intraepithelial neoplasia: biologic progression or independent lesions? Eur J Obstet Gynecol Reprod Biol 2005; 121 99–103.
Detection and typing of human papillomavirus DNA in uterine cervices with coexistent grade I and grade III intraepithelial neoplasia: biologic progression or independent lesions?CrossRef | 1:CAS:528:DC%2BD2MXlslylsL4%3D&md5=3e26366f06d56b6328b19d861117233cCAS | open url image1

[27]  De Vuyst H, Clifford GM, Nascimento MC, Madeleine MM, Franceschi S. Prevalence and type distribution of human papillomavirus in carcinoma and intraepithelial neoplasia of the vulva, vagina and anus: a meta-analysis. Int J Cancer 2009; 124 1626–36.
Prevalence and type distribution of human papillomavirus in carcinoma and intraepithelial neoplasia of the vulva, vagina and anus: a meta-analysis.CrossRef | 1:CAS:528:DC%2BD1MXivVars74%3D&md5=1ac1525531c054ca2c735a8bc85056aaCAS | open url image1

[28]  Gohy L, Gorska I, Rouleau D, Ghattas G, Pokomandy A, Vezina S, et al Genotyping of human papillomavirus DNA in anal biopsies and anal swabs collected from HIV-seropositive men with anal dysplasia. J Acquir Immune Defic Syndr 2008; 49 32–9.
Genotyping of human papillomavirus DNA in anal biopsies and anal swabs collected from HIV-seropositive men with anal dysplasia.CrossRef | 1:CAS:528:DC%2BD1cXhtVeis7vM&md5=4fe860227e1d3f5568e8622f1288abb5CAS | open url image1

[29]  Parkin DM, Bray F. Chapter 2: the burden of HPV-related cancers. Vaccine 2006; 24 11–25. open url image1

[30]  Hoots BE, Palefsky JM, Pimenta JM, Smith JS. Human papillomavirus type distribution in anal cancer and anal intraepithelial lesions. Int J Cancer 2009; 124 2375–83.
Human papillomavirus type distribution in anal cancer and anal intraepithelial lesions.CrossRef | 1:CAS:528:DC%2BD1MXltFaqtrk%3D&md5=134bfbdcad1e4cb8d06432e7489283e9CAS | open url image1

[31]  Darragh TM, Winkler B. Anal cancer and cervical cancer screening: key differences. Cancer cytopathology 2011 25 Feb; 119 5–19.
Anal cancer and cervical cancer screening: key differences.CrossRef | open url image1

[32]  Lina Villa L, Denny L. Chapter 7: methods for detection of HPV infection and its clinical utility. Int J Gynaecol Obstet 2006; 94 S71–80.
Chapter 7: methods for detection of HPV infection and its clinical utility.CrossRef | open url image1

[33]  Snijders PJ, Heideman DA, Meijer CJ. Methods for HPV detection in exfoliated cell and tissue specimens. APMIS 2010; 118 520–8.
Methods for HPV detection in exfoliated cell and tissue specimens.CrossRef | 1:CAS:528:DC%2BC3cXhtVSltb%2FP&md5=fb1f69a13c2a3e47231d01bfec8a7518CAS | open url image1

[34]  Molijn A, Kleter B, Quint W, van Doorn LJ. Molecular diagnosis of human papillomavirus (HPV) infections. J Clin Virol 2005; 32 S43–51.
Molecular diagnosis of human papillomavirus (HPV) infections.CrossRef | 1:CAS:528:DC%2BD2MXhvF2rtb8%3D&md5=b4e3f940a9314e2153b91acc518f40c1CAS | open url image1

[35]  Rebolj M, Bonde J, Njor SH, Lynge E. Human papillomavirus testing in primary cervical screening and the cut-off level for hybrid capture 2 tests: systematic review. BMJ 2011; 342 d2757
Human papillomavirus testing in primary cervical screening and the cut-off level for hybrid capture 2 tests: systematic review.CrossRef | open url image1

[36]  Pirotta MV, Stein AN, Fairley CK, Morrow A, Conway EL, Chuah J, et al Patterns of treatment of external genital warts in Australian sexual health clinics. Sex Transm Dis 2009; 36 375–9.
Patterns of treatment of external genital warts in Australian sexual health clinics.CrossRef | open url image1

[37]  Kyriakis KP, Hadjivassiliou M, Paparizos VA, Riga P, Katsambas A. Determinants of genital wart case detection rates among STD clinic attendees in Athens, Greece. Int J Dermatol 2005; 44 650–3.
Determinants of genital wart case detection rates among STD clinic attendees in Athens, Greece.CrossRef | open url image1

[38]  Jin F, Prestage GP, Kippax SC, Pell CM, Donovan B, Templeton DJ, et al Risk factors for genital and anal warts in a prospective cohort of HIV-negative homosexual men: the HIM study. Sex Transm Dis 2007; 34 488–93. open url image1

[39]  Wiley DJ, Grosser S, Qi K, Visscher BR, Beutner K, Strathdee SA, et al Validity of self-reporting of episodes of external genital warts. Clin Infect Dis 2002; 35 39–45.
Validity of self-reporting of episodes of external genital warts.CrossRef | 1:STN:280:DC%2BD38zhsleltA%3D%3D&md5=d547ef5cc449110f71b3f6fae34c8e8fCAS | open url image1

[40]  Smith JS, Gilbert PA, Melendy A, Rana RK, Pimenta JM. Age-specific prevalence of human papillomavirus infection in males: a global review. J Adolesc Health 2011; 48 540–52.
Age-specific prevalence of human papillomavirus infection in males: a global review.CrossRef | open url image1

[41]  Smith JS, Melendy A, Rana RK, Pimenta JM. Age-specific prevalence of infection with human papillomavirus in females: a global review. J Adolesc Health 2008 Oct; 43 S5–25. S e1–41. open url image1

[42]  Herrero R, Hildesheim A, Bratti C, Sherman ME, Hutchinson M, Morales J, et al Population-based study of human papillomavirus infection and cervical neoplasia in rural Costa Rica. J Natl Cancer Inst 2000; 92 464–74.
Population-based study of human papillomavirus infection and cervical neoplasia in rural Costa Rica.CrossRef | 1:STN:280:DC%2BD3c7otlOksw%3D%3D&md5=67d55096a3c03d71e031b7452f2993cbCAS | open url image1

[43]  Herrero R, Castle PE, Schiffman M, Bratti MC, Hildesheim A, Morales J, et al Epidemiologic profile of type-specific human papillomavirus infection and cervical neoplasia in Guanacaste, Costa Rica. J Infect Dis 2005; 191 1796–807.
Epidemiologic profile of type-specific human papillomavirus infection and cervical neoplasia in Guanacaste, Costa Rica.CrossRef | open url image1

[44]  Goldstone S, Palefsky JM, Giuliano AR, Moreira ED, Aranda C, Jessen H, et al Prevalence of and risk factors for human papillomavirus (HPV) infection among HIV-seronegative men who have sex with men. J Infect Dis 2011; 203 66–74.
Prevalence of and risk factors for human papillomavirus (HPV) infection among HIV-seronegative men who have sex with men.CrossRef | open url image1

[45]  Chin-Hong PV, Vittinghoff E, Cranston RD, Buchbinder S, Cohen D, Colfax G, et al Age-specific prevalence of anal human papillomavirus infection in HIV-negative sexually active men who have sex with men: the EXPLORE study. J Infect Dis 2004; 190 2070–6.
Age-specific prevalence of anal human papillomavirus infection in HIV-negative sexually active men who have sex with men: the EXPLORE study.CrossRef | open url image1

[46]  Vajdic CM, Van Leeuwen MT, Jin F, Prestage G, Medley G, Hillman RJ, et al Anal human papillomavirus genotype diversity and co-infection in a community-based sample of homosexual men. Sex Transm Infect 2009; 85 330–5.
Anal human papillomavirus genotype diversity and co-infection in a community-based sample of homosexual men.CrossRef | 1:STN:280:DC%2BD1MnjvFKjtw%3D%3D&md5=c2a0427ce6987600bd8acc290dde1ad2CAS | open url image1

[47]  Gao L, Zhou F, Li X, Yang Y, Ruan Y, Jin Q. Anal HPV infection in HIV-positive men who have sex with men from China. PLoS ONE 2010; 5 e15256
Anal HPV infection in HIV-positive men who have sex with men from China.CrossRef | 1:CAS:528:DC%2BC3cXhsFKlur%2FN&md5=d3ec9bf628b9864cdacd8713a8d7db5aCAS | open url image1

[48]  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 | open url image1

[49]  Grulich AE, de Visser RO, Smith AM, Rissel CE, Richters J. Sex in Australia: homosexual experience and recent homosexual encounters. Aust N Z J Public Health 2003; 27 155–63.
Sex in Australia: homosexual experience and recent homosexual encounters.CrossRef | open url image1

[50]  de Visser RO, Smith AM, Rissel CE, Richters J, Grulich AE. Sex in Australia: heterosexual experience and recent heterosexual encounters among a representative sample of adults. Aust N Z J Public Health 2003; 27 146–54.
Sex in Australia: heterosexual experience and recent heterosexual encounters among a representative sample of adults.CrossRef | open url image1

[51]  Guimarães MD, Grinsztejn B, Melo VH, Rocha GM, Campos LN, Pilotto JH, et al Anal HPV prevalence and associated factors among HIV-seropositive men under antiretroviral treatment in Brazil. J Acquir Immune Defic Syndr 2011; 57 S217–24.
Anal HPV prevalence and associated factors among HIV-seropositive men under antiretroviral treatment in Brazil.CrossRef | open url image1

[52]  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 | 1:STN:280:DC%2BD2crgslyrtw%3D%3D&md5=d428b4648c8095f957fff03999327872CAS | open url image1

[53]  Palefsky JM, Holly EA, Ralston ML, Jay N. Prevalence and risk factors for human papillomavirus infection of the anal canal in human immunodeficiency virus (HIV)-positive and HIV-negative homosexual men. J Infect Dis 1998; 177 361–7.
Prevalence and risk factors for human papillomavirus infection of the anal canal in human immunodeficiency virus (HIV)-positive and HIV-negative homosexual men.CrossRef | 1:STN:280:DyaK1c7isF2qug%3D%3D&md5=9307401f9018341d4be05af9f95c5583CAS | open url image1

[54]  Critchlow CW, Hawes SE, Kuypers JM, Goldbaum GM, Holmes KK, Surawicz CM, et al Effect of HIV infection on the natural history of anal human papillomavirus infection. AIDS 1998; 12 1177–84.
Effect of HIV infection on the natural history of anal human papillomavirus infection.CrossRef | 1:STN:280:DyaK1czjvFyhsw%3D%3D&md5=8cf67c40bf451fcd162af005e65fc7efCAS | open url image1

[55]  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 | 1:STN:280:DC%2BD3c%2FotlOhug%3D%3D&md5=02d5fb40c27c883b8f3fbfe7d496e504CAS | open url image1

[56]  Nielson CM, Harris RB, Flores R, Abrahamsen M, Papenfuss MR, Dunne EF, et al Multiple-type human papillomavirus infection in male anogenital sites: prevalence and associated factors. Cancer Epidemiol Biomarkers Prev 2009; 18 1077–83.
Multiple-type human papillomavirus infection in male anogenital sites: prevalence and associated factors.CrossRef | open url image1

[57]  Schiffman M, Wentzensen N, Wacholder S, Kinney W, Gage JC, Castle PE. Human papillomavirus testing in the prevention of cervical cancer. J Natl Cancer Inst 2011; 103 368–83.
Human papillomavirus testing in the prevention of cervical cancer.CrossRef | open url image1

[58]  Rodriguez AC, Burk R, Herrero R, Hildesheim A, Bratti C, Sherman ME, et al The natural history of human papillomavirus infection and cervical intraepithelial neoplasia among young women in the Guanacaste cohort shortly after initiation of sexual life. Sex Transm Dis 2007; 34 494–502. open url image1

[59]  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 | open url image1

[60]  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 | 1:CAS:528:DC%2BC3MXhsVSrsrbN&md5=5aa2abd713524740622154793fcda290CAS | open url image1

[61]  Safaeian M, Porras C, Schiffman M, Rodriguez AC, Wacholder S, Gonzalez P, et al Epidemiological study of anti-HPV16/18 seropositivity and subsequent risk of HPV16 and -18 infections. J Natl Cancer Inst 2010; 102 1653–62.
Epidemiological study of anti-HPV16/18 seropositivity and subsequent risk of HPV16 and -18 infections.CrossRef | 1:CAS:528:DC%2BC3cXhsVSlt7vM&md5=befa1a59f1e83e2ea8b30eb3ccdd56c3CAS | open url image1

[62]  Ho GY, Studentsov Y, Hall CB, Bierman R, Beardsley L, Lempa M, et al Risk factors for subsequent cervicovaginal human papillomavirus (HPV) infection and the protective role of antibodies to HPV-16 virus-like particles. J Infect Dis 2002; 186 737–42.
Risk factors for subsequent cervicovaginal human papillomavirus (HPV) infection and the protective role of antibodies to HPV-16 virus-like particles.CrossRef | open url image1

[63]  Malik ZA, Hailpern SM, Burk RD. Persistent antibodies to HPV virus-like particles following natural infection are protective against subsequent cervicovaginal infection with related and unrelated HPV. Viral Immunol 2009; 22 445–9.
Persistent antibodies to HPV virus-like particles following natural infection are protective against subsequent cervicovaginal infection with related and unrelated HPV.CrossRef | 1:CAS:528:DC%2BD1MXhs1Wht7fO&md5=3eb39e47dccdd4675ceb5c8af2e88e14CAS | open url image1

[64]  de Pokomandy A, Rouleau D, Ghattas G, Vezina S, Cote P, Macleod J, et al Prevalence, clearance, and incidence of anal human papillomavirus infection in HIV-infected men: the HIPVIRG cohort study. J Infect Dis 2009; 199 965–73.
Prevalence, clearance, and incidence of anal human papillomavirus infection in HIV-infected men: the HIPVIRG cohort study.CrossRef | open url image1

[65]  Poynten IM, Templeton DJ, Grulich AE. Sexually transmissible infections in aging HIV populations. Sex Health 2011; 8 508–11.
Sexually transmissible infections in aging HIV populations.CrossRef | open url image1

[66]  Shvetsov YB, Hernandez BY, McDuffie K, Wilkens LR, Zhu X, 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 | open url image1

[67]  Bhat P, Mattarollo SR, Gosmann C, Frazer IH, Leggatt GR. Regulation of immune responses to HPV infection and during HPV-directed immunotherapy. Immunol Rev 2011; 239 85–98.
Regulation of immune responses to HPV infection and during HPV-directed immunotherapy.CrossRef | 1:CAS:528:DC%2BC3MXhsVOgt7w%3D&md5=8c2f6b09942398d214deb76c51379607CAS | open url image1

[68]  Gravitt PE. The known unknowns of HPV natural history. J Clin Invest 2011; 121 4593–9.
The known unknowns of HPV natural history.CrossRef | 1:CAS:528:DC%2BC3MXhs1ShsLrN&md5=a766f3ef97c02700579a39dded925e2eCAS | open url image1

[69]  Strickler HD, Burk RD, Fazzari M, Anastos K, Minkoff H, Massad LS, et al Natural history and possible reactivation of human papillomavirus in human immunodeficiency virus-positive women. J Natl Cancer Inst 2005; 97 577–86.
Natural history and possible reactivation of human papillomavirus in human immunodeficiency virus-positive women.CrossRef | open url image1

[70]  Prestage G, Mao L, Fogarty A, Van de Ven P, Kippax S, Crawford J, et al How has the sexual behaviour of gay men changed since the onset of AIDS: 1986–2003. Aust N Z J Public Health 2005; 29 530–5.
How has the sexual behaviour of gay men changed since the onset of AIDS: 1986–2003.CrossRef | open url image1

[71]  Sapp M, Bienkowska-Haba M. Viral entry mechanisms: human papillomavirus and a long journey from extracellular matrix to the nucleus. FEBS J 2009; 276 7206–16.
Viral entry mechanisms: human papillomavirus and a long journey from extracellular matrix to the nucleus.CrossRef | 1:CAS:528:DC%2BD1MXhsFGqtr3I&md5=474104365696c96d22da3ad734557bd8CAS | open url image1

[72]  Haase AT. Targeting early infection to prevent HIV-1 mucosal transmission. Nature 2010; 464 217–23.
Targeting early infection to prevent HIV-1 mucosal transmission.CrossRef | 1:CAS:528:DC%2BC3cXjtFSmtrs%3D&md5=17d0c212bec3005162be0252dc5722f4CAS | open url image1

[73]  Palefsky J. Biology of HPV in HIV infection. Adv Dent Res 2006; 19 99–105.
Biology of HPV in HIV infection.CrossRef | 1:STN:280:DC%2BD283ksl2jtg%3D%3D&md5=9baf730cba54fcd020c2f143bb29bba3CAS | open url image1

[74]  Milošević M, Poljak M, Mlakar B. Anal HPV infection in Slovenian men who have sex with men. Cent Eur J Med 2010; 5 698–703.
Anal HPV infection in Slovenian men who have sex with men.CrossRef | open url image1

[75]  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 | 1:STN:280:DC%2BC3cbhtFOmtw%3D%3D&md5=69e6ad464e4e7e29cf987589aec24e90CAS | open url image1

[76]  Damay A, Fabre J, Costes V, Didelot JM, Didelot MN, Boulle N, et al Human papillomavirus (HPV) prevalence and type distribution, and HPV-associated cytological abnormalities in anal specimens from men infected with HIV who have sex with men. J Med Virol 2010; 82 592–6.
Human papillomavirus (HPV) prevalence and type distribution, and HPV-associated cytological abnormalities in anal specimens from men infected with HIV who have sex with men.CrossRef | open url image1

[77]  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 | open url image1



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