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RESEARCH ARTICLE
Contents Vol 9(6)

Prevalence and predictors of high-grade anal intraepithelial neoplasia in a community-based sample of homosexual men

Richard J. Hillman A F , Marina T. van Leeuwen B , Claire M. Vajdic C , Leo McHugh A , Garrett P. Prestage B , Leon P. Botes A , Iryna Zablotska B , Gabriele Medley D , Sepehr N. Tabrizi E , Andrew E. Grulich B and Fengyi Jin A
+ Author Affiliations
- Author Affiliations

A Sexually Transmitted Infections Research Centre, University of Sydney, Marion Villa, Westmead, NSW 2145, Australia.

B Kirby Institute, University of New South Wales, Darlinghurst, NSW 2010, Australia.

C Prince of Wales Clinical School and Lowy Cancer Research Centre, Faculty of Medicine, Building C25, Faculty of Medicine, Kensington Campus, University of New South Wales, NSW 2052, Australia.

D Melbourne Pathology, Private Bag 5, Collingwood, Vic. 3066, Australia.

E Department of Microbiology and Infectious Diseases, Bio 21 Institute, The Royal Women’s Hospital, Parkville, Vic. 3052, Australia.

F Corresponding author. Email: richard.hillman@sydney.edu.au

Sexual Health 9(6) 574-579 https://doi.org/10.1071/SH11139
Submitted: 7 March 2011  Accepted: 20 January 2012   Published: 11 May 2012

Abstract

Background: We report the prevalence and predictors for high-grade anal intraepithelial neoplasia (HGAIN) in community-based cohorts of HIV-negative and HIV-positive homosexual men in Sydney, Australia. Methods: A cross-sectional study of consecutive participants in both cohorts was performed in 2005 (204 HIV-negative and 128 HIV-positive men). Anal swabs collected by a research nurse underwent cytological analysis, using the ThinPrep procedure, and human papillomavirus (HPV) testing. Participants who had cytological abnormalities other than low-grade squamous epithelial lesions (SIL) were referred for high resolution anoscopy (HRA). Results: A total of 114 men had cytological abnormalities (24.3% of HIV-negative and 57.5% of HIV-positive men, odds ratio (OR) = 4.21, 95% confidence interval (CI) 2.57–6.90). However, only three (2.3%) HIV-positive men and no HIV-negative men had high-grade SIL on anal cytology. Seventy-seven men were referred for HRA, of whom 63 (81.8%) attended. Histologically confirmed HGAIN was detected in 21 (33.3%). The prevalence of HGAIN was higher in HIV-positive men (10.8%) than in HIV-negative men (5.0%, OR = 2.29, 95% CI 0.93–5.63, P = 0.071). HGAIN was not related to age but was strongly associated with the detection of high-risk types of anal HPV (OR = 10.1, 95% CI 1.33–76.2) rather than low-risk types (OR = 1.97, 95% CI 0.74–5.25). Conclusion: HGAIN was prevalent in homosexual men across all age groups and was more than twice as common in HIV-positive men compared with HIV-negative men. The presence of high-risk anal HPV was highly predictive of HGAIN.

Additional keywords: Australia, HPV, risk factor.


References

[1]  Johnson LG, Madeleine MM, Newcomer LM, Schwartz SM, Daling JR. Anal cancer incidence and survival: the surveillance, epidemiology, and end results experience, 1973–2000. Cancer 2004; 101 281–8.
| Anal cancer incidence and survival: the surveillance, epidemiology, and end results experience, 1973–2000.Crossref | GoogleScholarGoogle Scholar | 15241824PubMed |

[2]  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 | GoogleScholarGoogle Scholar | 18980293PubMed |

[3]  Robinson D, Coupland V, Moller H. An analysis of temporal and generational trends in the incidence of anal and other HPV-related cancers in Southeast England. Br J Cancer 2009; 100 527–31.
| An analysis of temporal and generational trends in the incidence of anal and other HPV-related cancers in Southeast England.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M7hs1Oqtw%3D%3D&md5=fcf13ed62ec1d3318ac9798cea8f9346CAS | 19156144PubMed |

[4]  Brewster DH, Bhatti LA. Increasing incidence of squamous cell carcinoma of the anus in Scotland, 1975–2002. Br J Cancer 2006; 95 87–90.
| Increasing incidence of squamous cell carcinoma of the anus in Scotland, 1975–2002.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zos1ynsQ%3D%3D&md5=9fd6102fe045700cc5618102f0db1630CAS | 16721368PubMed |

[5]  Australian Institute of Health and Welfare. Number of new cases and age-standardised rates (Australia 2001 and World) for selected cancers by year and sex, Australia, 1982–2005. In. Canberra: Australian Institute of Health and Welfare, Canberra; 2009.

[6]  Parkin DM, Bray F. Chapter 2: The burden of HPV-related cancers. Vaccine 2006,24 Suppl 3:S3/11-25.

[7]  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 | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7isF2qug%3D%3D&md5=9307401f9018341d4be05af9f95c5583CAS | 9466522PubMed |

[8]  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 | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c%2FhsVSgtg%3D%3D&md5=651553935aeed99ac143a7b52879ed1bCAS | 2821396PubMed |

[9]  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 | GoogleScholarGoogle Scholar | 18614927PubMed |

[10]  Peto J, Gilham C, Fletcher O, Matthews FE. The cervical cancer epidemic that screening has prevented in the UK. Lancet 2004; 364 249–56.
| The cervical cancer epidemic that screening has prevented in the UK.Crossref | GoogleScholarGoogle Scholar | 15262102PubMed |

[11]  Vizcaino AP, Moreno V, Bosch FX, Munoz N, Barros-Dios XM, Borras J, et al International trends in incidence of cervical cancer: II. Squamous-cell carcinoma. Int J Cancer 2000; 86 429–35.
| International trends in incidence of cervical cancer: II. Squamous-cell carcinoma.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3isFOqsQ%3D%3D&md5=e4ed852420b0b25dd36d3eb858adf327CAS | 10760834PubMed |

[12]  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 |

[13]  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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFaqtrk%3D&md5=134bfbdcad1e4cb8d06432e7489283e9CAS | 19189402PubMed |

[14]  Noffsinger A, Witte D, Fenoglio-Preiser CM. The relationship of human papillomaviruses to anorectal neoplasia. Cancer 1992; 70 1276–87.
| The relationship of human papillomaviruses to anorectal neoplasia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38znvFOjtg%3D%3D&md5=5d1b1af480ba2c7f37fe23d65272740fCAS | 1324782PubMed |

[15]  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 | GoogleScholarGoogle Scholar | 20719211PubMed |

[16]  Palefsky JM, Holly EA, Hogeboom CJ, Berry JM, Jay N, Darragh TM. Anal cytology as a screening tool for anal squamous intraepithelial lesions. J Acquir Immune Defic Syndr Hum Retrovirol 1997; 14 415–22.
| Anal cytology as a screening tool for anal squamous intraepithelial lesions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szhsVSksQ%3D%3D&md5=843dc3a3960718701c4eb9321b89291cCAS | 9170415PubMed |

[17]  Anderson JS, Vajdic C, Grulich AE. Is screening for anal cancer warranted in homosexual men? Sex Health 2004; 1 137–40.
| Is screening for anal cancer warranted in homosexual men?Crossref | GoogleScholarGoogle Scholar | 16335300PubMed |

[18]  Goldie SJ, Kuntz KM, Weinstein MC, Freedberg KA, Palefsky JM. Cost-effectiveness of screening for anal squamous intraepithelial lesions and anal cancer in human immunodeficiency virus-negative homosexual and bisexual men. Am J Med 2000; 108 634–41.
| Cost-effectiveness of screening for anal squamous intraepithelial lesions and anal cancer in human immunodeficiency virus-negative homosexual and bisexual men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3czhsFKkuw%3D%3D&md5=9f4a6ebb72cf5ff4301b50ed8298649cCAS | 10856411PubMed |

[19]  Goldie SJ, Kuntz KM, Weinstein MC, Freedberg KA, Welton ML, Palefsky JM. The clinical effectiveness and cost-effectiveness of screening for anal squamous intraepithelial lesions in homosexual and bisexual HIV-positive men. JAMA 1999; 281 1822–9.
| The clinical effectiveness and cost-effectiveness of screening for anal squamous intraepithelial lesions in homosexual and bisexual HIV-positive men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M3ntVWqtw%3D%3D&md5=c47329bf0031fbe3862cbb4f832abfa9CAS | 10340370PubMed |

[20]  Jin F, Prestage GP, Mao L, Kippax SC, Pell CM, Donovan B, et al Transmission of herpes simplex virus types 1 and 2 in a prospective cohort of HIV-negative gay men: the Health in Men study. J Infect Dis 2006; 194 561–70.
| Transmission of herpes simplex virus types 1 and 2 in a prospective cohort of HIV-negative gay men: the Health in Men study.Crossref | GoogleScholarGoogle Scholar | 16897652PubMed |

[21]  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 | GoogleScholarGoogle Scholar | 16370050PubMed |

[22]  National Health and Medical Research Council. Screening to prevent cervical cancer: guidelines for the management of asymptomatic women with screen detected abnormalities In. Canberra: Commonwealth of Australia; 2005.

[23]  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 | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MnjvFKjtw%3D%3D&md5=c2a0427ce6987600bd8acc290dde1ad2CAS | 19342375PubMed |

[24]  Friedman HB, Saah AJ, Sherman ME, Busseniers AE, Blackwelder WC, Kaslow RA, et al Human papillomavirus, anal squamous intraepithelial lesions, and human immunodeficiency virus in a cohort of gay men. J Infect Dis 1998; 178 45–52.
| 1:STN:280:DyaK1czhsVGgsg%3D%3D&md5=40931e7c96cca42d6c0bff031e844311CAS | 9652422PubMed |

[25]  Kiviat NB, Critchlow CW, Holmes KK, Kuypers J, Sayer J, Dunphy C, et al Association of anal dysplasia and human papillomavirus with immunosuppression and HIV infection among homosexual men. AIDS 1993; 7 43–50.
| Association of anal dysplasia and human papillomavirus with immunosuppression and HIV infection among homosexual men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s7otlCgsQ%3D%3D&md5=cc39aed15be2d0d400de9495afe553d7CAS | 8382927PubMed |

[26]  Palefsky JM, Holly EA, Ralston ML, Arthur SP, Jay N, Berry JM, et al Anal squamous intraepithelial lesions in HIV-positive and HIV-negative homosexual and bisexual men: prevalence and risk factors. J Acquir Immune Defic Syndr Hum Retrovirol 1998; 17 320–6.
| Anal squamous intraepithelial lesions in HIV-positive and HIV-negative homosexual and bisexual men: prevalence and risk factors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7osVentg%3D%3D&md5=836987e9a63dc0fd9802b69397daa436CAS | 9525432PubMed |

[27]  Chin-Hong PV, Vittinghoff E, Cranston RD, Browne L, Buchbinder S, Colfax G, et al Age-related prevalence of anal cancer precursors in homosexual men: the EXPLORE study. J Natl Cancer Inst 2005; 97 896–905.
| Age-related prevalence of anal cancer precursors in homosexual men: the EXPLORE study.Crossref | GoogleScholarGoogle Scholar | 15956651PubMed |

[28]  Berry JM, Palefsky JM, Jay N, Cheng SC, Darragh TM, Chin-Hong PV. Performance characteristics of anal cytology and human papillomavirus testing in patients with high-resolution anoscopy-guided biopsy of high-grade anal intraepithelial neoplasia. Dis Colon Rectum 2009; 52 239–47.
| Performance characteristics of anal cytology and human papillomavirus testing in patients with high-resolution anoscopy-guided biopsy of high-grade anal intraepithelial neoplasia.Crossref | GoogleScholarGoogle Scholar | 19279418PubMed |

[29]  Anderson J, Hoy J, Hillman R, Gittleson C, Hartel G, Medley G, et al Abnormal anal cytology in high-risk human papilloma virus infection in HIV-infected Australians. Sex Transm Infect 2008; 84 94–6.
| Abnormal anal cytology in high-risk human papilloma virus infection in HIV-infected Australians.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c3htVSmuw%3D%3D&md5=2bfa28cbd939a65ec681d90d783f5648CAS | 17881414PubMed |

[30]  Kreuter A, Brockmeyer NH, Weissenborn SJ, Gambichler T, Stucker M, Altmeyer P, et al Penile intraepithelial neoplasia is frequent in HIV-positive men with anal dysplasia. J Invest Dermatol 2008; 128 2316–24.
| Penile intraepithelial neoplasia is frequent in HIV-positive men with anal dysplasia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpslWns7k%3D&md5=1915ffa19f441633b3006c1ab04abab9CAS | 18385760PubMed |

[31]  Piketty C, Darragh TM, Heard I, Da Costa M, Bruneval P, Kazatchkine MD, et al High prevalence of anal squamous intraepithelial lesions in HIV-positive men despite the use of highly active antiretroviral therapy. Sex Transm Dis 2004; 31 96–9.
| High prevalence of anal squamous intraepithelial lesions in HIV-positive men despite the use of highly active antiretroviral therapy.Crossref | GoogleScholarGoogle Scholar | 14743072PubMed |

[32]  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 |

[33]  New York State Department of Public Health AIDS Institute. Clinical Guidelines: Neoplastic Complications of HIV Infection; Section V – Anal Dysplasia and Cancer. 2007.

[34]  Frisch M, Glimelius B, van den Brule AJ, Wohlfahrt J, Meijer CJ, Walboomers JM, et al Sexually transmitted infection as a cause of anal cancer. N Engl J Med 1997; 337 1350–8.
| Sexually transmitted infection as a cause of anal cancer.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FgtVSjtg%3D%3D&md5=85b48368c0091b3841291d9bd7f8096cCAS | 9358129PubMed |

[35]  Salit IE, Lytwyn A, Raboud J, Sano M, Chong S, Diong C, et al The role of cytology (Pap tests) and human papillomavirus testing in anal cancer screening. AIDS 2010; 24 1307–13.
| 20442633PubMed |

[36]  Salit IE, Tinmouth J, Chong S, Raboud J, Diong C, Su D, et al Screening for HIV-associated anal cancer: correlation of HPV genotypes, p16, and E6 transcripts with anal pathology. Cancer Epidemiol Biomarkers Prev 2009; 18 1986–92.
| Screening for HIV-associated anal cancer: correlation of HPV genotypes, p16, and E6 transcripts with anal pathology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFWjsrw%3D&md5=2e0b1548b539209aef6a9f3fbf8c40e9CAS | 19567510PubMed |

[37]  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 | GoogleScholarGoogle Scholar | 15551204PubMed |