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RESEARCH ARTICLE

Epidemiology, natural history and risk factors for anal intraepithelial neoplasia

François Coutlée A B C F , Alexandra de Pokomandy D E and Eduardo L. Franco C
+ Author Affiliations
- Author Affiliations

A Départements de Microbiologie et Infectiologie, Centre Hospitalier de l’Université de Montréal, Montreal, Quebec H2L 4M1, Canada.

B Département de Microbiologie et Immunologie, Université de Montréal, Montreal, Quebec H3T IJ4, Canada.

C Division of Cancer Epidemiology, McGill University, Montreal, Quebec H2W 1S6, Canada.

D Department of Medicine, Immunodeficiency Service, McGill University Health Centre, Montreal, Quebec H2X 2P4, Canada.

E Department of Family Medicine, McGill University, Montreal, Quebec H2X 2P4, Canada.

F Corresponding author. Email: francois.coutlee@ssss.gouv.qc.ca

Sexual Health 9(6) 547-555 https://doi.org/10.1071/SH11167
Submitted: 30 November 2011  Accepted: 7 February 2012   Published: 8 June 2012

Abstract

Studies conducted in HIV-seropositive individuals have enhanced our understanding of the natural history of anal intraepithelial neoplasia (AIN) and of factors predictive of progression to high-grade AIN, the immediate precursor to anal cancer. AIN is frequently detected in HIV-seropositive individuals. Factors that increase the risk for AIN include HIV infection, low current or nadir blood CD4+ cell counts, receptive anal intercourse, oncogenic human papillomavirus (HPV) infection, persistent anal HPV infection, multiple HPV type infections and high anal HPV viral load. This review confirms the importance of high-grade AIN in HIV-seropositive individuals and HIV-seronegative men having sex with men.

Additional keywords: HIV, human papillomavirus, intraepithelial lesions, men who have sex with men.


References

[1]  Frisch M, Biggar IJ, Goedert JJ. Human papillomavirus-associated cancers in patients with human immunodeficiency virus infection and acquired immunodeficiency syndrome. J Natl Cancer Inst 2000; 92 1500–10.
Human papillomavirus-associated cancers in patients with human immunodeficiency virus infection and acquired immunodeficiency syndrome.Crossref | GoogleScholarGoogle Scholar | 10995805PubMed |

[2]  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 | 9543448PubMed |

[3]  Bower M, Powles T, Newsom Davis T, Thirlwell C, Stebbing J, Mandalia S, et al HIV-associated anal cancer: has highly active antiretroviral therapy reduced the incidence or improved the outcome? J Acquir Immune Defic Syndr 2004; 37 1563–5.
HIV-associated anal cancer: has highly active antiretroviral therapy reduced the incidence or improved the outcome?Crossref | GoogleScholarGoogle Scholar | 15577408PubMed |

[4]  Palefsky JM. Human papillomavirus infection and anogenital neoplasia in human immunodeficiency virus-positive men and women. J Natl Cancer Inst 1998; 23 15–20.

[5]  Palefsky JM. Anal squamous intraepithelial lesions: relation to HIV and human papillomavirus infection. J Acquir Immun Defic Syndr 1999; 21 S42–8.

[6]  Powles T, Robinson D, Stebbing J, Sharmash J, Nelson M, Gazzard B, et al Highly active antiretroviral therapy and the incidence of non-AIDS-defining cancers in people with HIV infection. J Clin Oncol 2009; 27 884–90.
Highly active antiretroviral therapy and the incidence of non-AIDS-defining cancers in people with HIV infection.Crossref | GoogleScholarGoogle Scholar | 19114688PubMed |

[7]  Chaturvedi AK, Madeleine MM, Biggar RJ, Engels EA. Risk of human papillomavirus-associated cancers among persons with AIDS. J Natl Cancer Inst 2009; 101 1120–30.
Risk of human papillomavirus-associated cancers among persons with AIDS.Crossref | GoogleScholarGoogle Scholar | 19648510PubMed |

[8]  Fang CT, Chang YY, Hsu HM, Twu SJ, Chen KT, Lin CC, et al Life expectancy of patients with newly-diagnosed HIV infection in the era of highly active antiretroviral therapy. QJM 2007; 100 97–105.
Life expectancy of patients with newly-diagnosed HIV infection in the era of highly active antiretroviral therapy.Crossref | GoogleScholarGoogle Scholar | 17277317PubMed |

[9]  Piketty C, Selinger Leneman H, Grabar S, Duvivier C, Bonmarchand M, Abramowitz L, et al Marked increase in the incidence of invasive anal cancer among HIV-infected patients despite treatment with combination antiretroviral therapy. AIDS 2008; 22 1203–11.
Marked increase in the incidence of invasive anal cancer among HIV-infected patients despite treatment with combination antiretroviral therapy.Crossref | GoogleScholarGoogle Scholar | 18525266PubMed |

[10]  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 |

[11]  Mathews WC. Screening for anal dysplasia associated with human papillomavirus. Top HIV Med 2003; 11 45–9.
| 12717041PubMed |

[12]  Palefsky JM. Cervical human papillomavirus infection and cervical intraepithelial neoplasia in women positive for human immunodeficiency virus in the era of highly active antiretroviral therapy. Curr Opin Oncol 2003; 15 382–8.
Cervical human papillomavirus infection and cervical intraepithelial neoplasia in women positive for human immunodeficiency virus in the era of highly active antiretroviral therapy.Crossref | GoogleScholarGoogle Scholar | 12960521PubMed |

[13]  Zbar AP, Fenger C, Efron J, Beer-Gabel M, Wexner SD. The pathology and molecular biology of anal intraepithelial neoplasia: comparisons with cervical and vulvar intraepithelial carcinoma. Int J Colorectal Dis 2002; 17 203–15.
The pathology and molecular biology of anal intraepithelial neoplasia: comparisons with cervical and vulvar intraepithelial carcinoma.Crossref | GoogleScholarGoogle Scholar | 12073068PubMed |

[14]  Fox PA. human papillomavirus and anal intraepithelial neoplasia. Curr Opinions Inf Dis 2006; 19 62–6.
human papillomavirus and anal intraepithelial neoplasia.Crossref | GoogleScholarGoogle Scholar |

[15]  Darragh TM, Winkler B. Anal cancer and cervical cancer screening: key differences. Cancer 2011; 119 5–19.
Anal cancer and cervical cancer screening: key differences.Crossref | GoogleScholarGoogle Scholar |

[16]  Goldstone SE, Winkler B, Ufford LJ, Alt E, Palefsky JM. High prevalence of anal squamous intraepithelial lesions and squamous cell carcinoma in men who have sex with men as seen in a surgical practice. Dis Colon Rectum 2001; 44 690–8.
High prevalence of anal squamous intraepithelial lesions and squamous cell carcinoma in men who have sex with men as seen in a surgical practice.Crossref | GoogleScholarGoogle Scholar | 11357031PubMed |

[17]  Chin-Hong PV, Palefsky JM. Natural history and clinical management of anal human papillomavirus disease in men and women infected with human immunodeficiency virus. Clin Infect Dis 2002; 35 1127–34.
Natural history and clinical management of anal human papillomavirus disease in men and women infected with human immunodeficiency virus.Crossref | GoogleScholarGoogle Scholar | 12384848PubMed |

[18]  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 | 9358129PubMed |

[19]  Moscicki AB, Palefsky JM. Human papillomavirus in men: an update. J Low Genit Tract Dis 2011; 15 231–4.
Human papillomavirus in men: an update.Crossref | GoogleScholarGoogle Scholar | 21543996PubMed |

[20]  de Sanjosé S, Palefsky J. Cervical and anal HPV infections in HIV positive women and men. Virus Res 2002; 89 201–11.
Cervical and anal HPV infections in HIV positive women and men.Crossref | GoogleScholarGoogle Scholar | 12445660PubMed |

[21]  Kreuter A, Potthoff A, Brockmeyer NH, Gambichler T, Swoboda J, Stucker M, et al Anal carcinoma in human immunodeficiency virus-positive men: results of a prospective study from Germany. Br J Dermatol 2010; 162 1269–77.
Anal carcinoma in human immunodeficiency virus-positive men: results of a prospective study from Germany.Crossref | GoogleScholarGoogle Scholar | 20184584PubMed |

[22]  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 | GoogleScholarGoogle Scholar | 16916390PubMed |

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

[24]  Chiao EY, Giordano TP, Palefsky JM, Tyring S, El-Serag H. Screening HIV-infected individuals for anal cancer precursor lesions: a systematic review. Clin Infect Dis 2006; 43 223–33.
Screening HIV-infected individuals for anal cancer precursor lesions: a systematic review.Crossref | GoogleScholarGoogle Scholar | 16779751PubMed |

[25]  Weis SE, Vecino I, Pogoda JM, Susa JS, Nevoit J, Radaford D, et al Prevalence of anal intraepithelial neoplasia defined by anal cytology screening and high-resolution anoscopy in a primary care population of HIV-infected men and women. Dis Colon Rectum 2011; 54 433–41.
Prevalence of anal intraepithelial neoplasia defined by anal cytology screening and high-resolution anoscopy in a primary care population of HIV-infected men and women.Crossref | GoogleScholarGoogle Scholar | 21383563PubMed |

[26]  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 | 20925532PubMed |

[27]  Lacey HB, Wilson GE, Tilston P, Wilkins EG, Bailey AS, Corbitt G, et al A study of anal intraepithelial neoplasia in HIV positive homosexual men. Sex Transm Infect 1999; 75 172–7.
A study of anal intraepithelial neoplasia in HIV positive homosexual men.Crossref | GoogleScholarGoogle Scholar | 10448395PubMed |

[28]  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 | 10340370PubMed |

[29]  Palefsky JM, Holly EA, Ralston ML, Arthur SP, Hogeboom CJ, Darragh TM. Anal cytological abnormalities and anal HPV infection in men with Centers for Disease Control group IV HIV disease. Genitourin Med 1997; 73 174–80.
| 9306896PubMed |

[30]  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 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 |

[31]  Salit I, Tinmouth J, Chong S, Raboud J, Diong C, Su D. 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 | 19567510PubMed |

[32]  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 43–9.
Association of anal dysplasia and human papillomavirus with immunosuppression and HIV infection among homosexual men.Crossref | GoogleScholarGoogle Scholar | 8382927PubMed |

[33]  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 |

[34]  Tilston P. Anal human papillomavirus and anal cancer. J Clin Pathol 1997; 50 625–34.
Anal human papillomavirus and anal cancer.Crossref | GoogleScholarGoogle Scholar | 9301544PubMed |

[35]  Nathan M, Singh N, Garrett N, Hickey N, Prevost T, Sheaff M. Performance of anal cytology in a clinical setting when measured against histology and high-resolution anoscopy findings. AIDS 2010; 24 373–9.
Performance of anal cytology in a clinical setting when measured against histology and high-resolution anoscopy findings.Crossref | GoogleScholarGoogle Scholar | 20057313PubMed |

[36]  Palefsky JM, Holly EA, Gonzales J, Lamborn K, Hollander H. Natural history of anal cytologic abnormalities and papillomavirus infection among homosexual men with group IV HIV disease. J Acquir Immune Defic Syndr 1992; 5 1258–65.
Natural history of anal cytologic abnormalities and papillomavirus infection among homosexual men with group IV HIV disease.Crossref | GoogleScholarGoogle Scholar | 1333531PubMed |

[37]  Palefsky JM, Holly EA, Hogeboom CJ, Ralston ML, DaCosta MM, Botts R, et al Virologic, immunologic, and clinical parameters in the incidence and progression of anal squamous intraepithelial lesions in HIV-positive and HIV-negative homosexual men. J Acquir Immune Defic Syndr 1998; 17 314–9.
Virologic, immunologic, and clinical parameters in the incidence and progression of anal squamous intraepithelial lesions in HIV-positive and HIV-negative homosexual men.Crossref | GoogleScholarGoogle Scholar |

[38]  Critchlow CW, Surawicz CM, Holmes KK, Kuypers J, Daling JR, Hawes SE, et al Prospective study of high grade anal squamous intraepithelial neoplasia in a cohort of homosexual men: Influence of HIV infection, immunosuppression and human papillomavirus infection. AIDS 1995; 9 1255–62.
Prospective study of high grade anal squamous intraepithelial neoplasia in a cohort of homosexual men: Influence of HIV infection, immunosuppression and human papillomavirus infection.Crossref | GoogleScholarGoogle Scholar | 8561979PubMed |

[39]  Abramowitz L, Benabderrahmane D, Ravaud P, Walker F, Rioux C, Jestin C, et al Anal squamous intraepithelial lesions and condyloma in HIV-infected heterosexual men, homosexual men and women: prevalence and associated factors. AIDS 2007; 21 1457–65.
Anal squamous intraepithelial lesions and condyloma in HIV-infected heterosexual men, homosexual men and women: prevalence and associated factors.Crossref | GoogleScholarGoogle Scholar | 17589192PubMed |

[40]  Abramowitz L, Benabderrahmane D, Baron G, Walker F, Yeni P, Duval X. Systematic evaluation and description of anal pathology in HIV-infected patients during the HAART era. Dis Colon Rectum 2009; 52 1130–6.
Systematic evaluation and description of anal pathology in HIV-infected patients during the HAART era.Crossref | GoogleScholarGoogle Scholar | 19581857PubMed |

[41]  Sobhani I, Vuagnat A, Walker F, Vissuzaine C, Mirin B, Hervatin F, et al Prevalence of high-grade dysplasia and cancer in the anal canal in human papillomavirus-infected individuals. Gastroenterology 2001; 120 857–66.
Prevalence of high-grade dysplasia and cancer in the anal canal in human papillomavirus-infected individuals.Crossref | GoogleScholarGoogle Scholar | 11231940PubMed |

[42]  Wang C, Wright TC, Denny L, Kuhn L. Rapid rise in detection of human papillomavirus (HPV) infection soon after incident HIV infection among South African women. J Infect Dis 2011; 203 479–86.
Rapid rise in detection of human papillomavirus (HPV) infection soon after incident HIV infection among South African women.Crossref | GoogleScholarGoogle Scholar | 21216869PubMed |

[43]  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 |

[44]  Park IU, Palefsky JM. Evaluation and Management of Anal Intraepithelial Neoplasia in HIV-Negative and HIV-Positive Men Who Have Sex with Men. Curr Infect Dis Rep 2010; 12 126–33.
Evaluation and Management of Anal Intraepithelial Neoplasia in HIV-Negative and HIV-Positive Men Who Have Sex with Men.Crossref | GoogleScholarGoogle Scholar | 20461117PubMed |

[45]  Chin Hong PV, Berry JM, Cheng SC, Catania JA, Da Costa M, Darragh TM, et al Comparison of patient- and clinician-collected anal cytology samples to screen for human papillomavirus-associated anal intraepithelial neoplasia in men who have sex with men. Ann Intern Med 2008; 149 300–6.
| 18765699PubMed |

[46]  Piketty C, Darragh TM, Da Costa M, Bruneval P, Heard I, Kazatchkine MD. 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 |

[47]  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 |

[48]  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 |

[49]  Shiels MS, Cole SR, Kirk GD, Poole C. A meta-analysis of the incidence of non-AIDS cancers in HIV-infected individuals. J Acquir Immune Defic Syndr 2009; 52 611–22.
A meta-analysis of the incidence of non-AIDS cancers in HIV-infected individuals.Crossref | GoogleScholarGoogle Scholar | 19770804PubMed |

[50]  Hessol NA, Holly EA, Efird JT, Minkoff H, Schowalter K, Darragh TM, 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 |

[51]  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 | 11390533PubMed |

[52]  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 |

[53]  Palefsky JM, Holly EA, Ralston ML, DaCosta MM, Greenblatt RM. Prevalence and risk factors for anal human papillomavirus infection in Human immunodeficiency (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 (HIV)-positive and high risk HIV-negative women.Crossref | GoogleScholarGoogle Scholar | 11133369PubMed |

[54]  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.
| 8290181PubMed |

[55]  Tandon R, Baranoski AS, Huang F, las Morenas A, Vragovic O, Sullivan M, et al Abnormal anal cytology in HIV-infected women. Am J Obstet Gynecol 2010; 203 21.e1–21.e6.
Abnormal anal cytology in HIV-infected women.Crossref | GoogleScholarGoogle Scholar |

[56]  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
HPV type infection in different anogenital sites among HIV-positive Brazilian women.Crossref | GoogleScholarGoogle Scholar | 18341690PubMed |

[57]  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.
| 8970684PubMed |

[58]  Melbye M, Smith E, Wohlfahrt J, Osterlind A, Orholm M, Bergmann OJ, et al Anal and cervical abnormality in women - prediction by human papillomavirus tests. Int J Cancer 1996; 68 559–64.
Anal and cervical abnormality in women - prediction by human papillomavirus tests.Crossref | GoogleScholarGoogle Scholar | 8938134PubMed |

[59]  Poizot-Martin I, Henry M, Benhaim S, Obry Roguet V, Figarella D, Tamalet C. High level of HPV 16 and 18 DNA load in anal swabs from male and female HIV-1 infected patients. J Clin Virol 2009; 44 314–7.
High level of HPV 16 and 18 DNA load in anal swabs from male and female HIV-1 infected patients.Crossref | GoogleScholarGoogle Scholar | 19269245PubMed |

[60]  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 |

[61]  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 |

[62]  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 | 19189402PubMed |

[63]  Gohy L, Gorska I, de Pokomandy A, Rouleau D, Ghattas G, Allaire G, et al Genotyping of Human papillomavirus in anal biopsies and anal swabs collected from HIV-seropositive men with anal dysplasia. J Acquir Immun Defic Syndr 2008; 49 32–9.
Genotyping of Human papillomavirus in anal biopsies and anal swabs collected from HIV-seropositive men with anal dysplasia.Crossref | GoogleScholarGoogle Scholar |

[64]  Martin F, Bower M. Anal intraepithelial neoplasia in HIV positive people. Sex Transm Infect 2001; 77 327–31.
Anal intraepithelial neoplasia in HIV positive people.Crossref | GoogleScholarGoogle Scholar | 11588276PubMed |

[65]  Palefsky JM, Shiboski S, Moss A. Risk factors for anal human papillomavirus infection and anal cytologic abnormalities in HIV-positive and HIV-seronegative homosexual men. J Acquir Immune Defic Syndr 1994; 7 599–606.
| 8176644PubMed |

[66]  Palefsky JL, Gonzales J, Greenblatt RM, Ahn DK, Hollander H. Anal intraepithelial neoplasia and anal papillomavirus infection among homosexual males with group IV disease. JAMA 1990; 263 2911–6.
Anal intraepithelial neoplasia and anal papillomavirus infection among homosexual males with group IV disease.Crossref | GoogleScholarGoogle Scholar |

[67]  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.
| 9652422PubMed |

[68]  Ryan DP, Compton CC, Mayer RJ. Carcinoma of the anal canal. N Engl J Med 2000; 342 792–800. [Review] [125 refs]
Carcinoma of the anal canal.Crossref | GoogleScholarGoogle Scholar | 10717015PubMed |

[69]  Frazer IH, Medley G, Crapper RM, Brown TC, Mackay IR. Association between anorectal dysplasia, human papillomavirus, and human immunodeficiency virus infection in homosexual men. Lancet 1986; 328 657–60.
Association between anorectal dysplasia, human papillomavirus, and human immunodeficiency virus infection in homosexual men.Crossref | GoogleScholarGoogle Scholar |

[70]  Law CL, Qassim M, Thompson CH, Rose BR, Grace J, Morris BJ, et al Factors associated with clinical and sub-clinical anal human papillomavirus infection in homosexual men. Genitourin Med 1991; 67 92–8.
| 1851723PubMed |

[71]  Sonnex C, Scholefield JH, Kocjan G, Kelly G, Whatrup C, Mindel A, et al Anal human papillomavirus infection: a comparative study of cytology, colposcopy and DNA hybridisation as methods of detection. Genitourin Med 1991; 67 21–5.
| 1655621PubMed |

[72]  Xi LF, Critchlow CW, Wheeler CM, Koutsky LA, Galloway DA, Kuypers J, et al Risk of anal carcinoma in situ in relation to human papillomavirus type 16 variants. Cancer Res 1998; 58 3839–44.
| 9731493PubMed |

[73]  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 | 9466522PubMed |

[74]  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 | GoogleScholarGoogle Scholar | 19239366PubMed |

[75]  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 | GoogleScholarGoogle Scholar | 9677167PubMed |

[76]  Rowhani-Rahbar A, Hawes SE, Sow PS, Toure P, Feng Q, Dem A, et al The impact of HIV status and type on the clearance of human papillomavirus infection among Senegalese women. J Infect Dis 2007; 196 887–94.
The impact of HIV status and type on the clearance of human papillomavirus infection among Senegalese women.Crossref | GoogleScholarGoogle Scholar | 17703420PubMed |

[77]  Alvarez J, de Pokomandy A, Rouleau D, Ghattas G, Vezina S, Cote P, et al Episomal and integrated Human papillomavirus type 16 loads and anal intraepithelial neoplasia in HIV-seropositive men. AIDS 2010; 24 2355–63.
| 20706109PubMed |

[78]  Da Costa MM, Hogeboom CJ, Holly EA, Palefsky JM. Increased risk of high-grade anal neoplasia associated with a human papillomavirus type 16 E6 sequence variant. J Infect Dis 2002; 185 1229–37.
Increased risk of high-grade anal neoplasia associated with a human papillomavirus type 16 E6 sequence variant.Crossref | GoogleScholarGoogle Scholar | 12001039PubMed |

[79]  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 | 15478076PubMed |

[80]  Palefsky JM, Holly EA, Efirdc JT, Da-Costa M, Jay N, Berry JM, et al Anal intraepithelial neoplasia in the highly active antiretroviral therapy era among HIV-positive men who have sex with men. AIDS 2005; 19 1407–14.
Anal intraepithelial neoplasia in the highly active antiretroviral therapy era among HIV-positive men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 16103772PubMed |

[81]  Ciobotaru B, Leiman G, St John T, Hyman N, Ramundo M, Grace C. Prevalence and risk factors for anal cytologic abnormalities and human papillomavirus infection in a rural population of HIV-infected males. Dis Colon Rectum 2007; 50 1011–6.
Prevalence and risk factors for anal cytologic abnormalities and human papillomavirus infection in a rural population of HIV-infected males.Crossref | GoogleScholarGoogle Scholar | 17429713PubMed |

[82]  Hogg RS, Yip B, Chan KJ, Wood E, Craib KJ, O’Shaughnessy MV, et al Rates of disease progression by baseline CD4 cell count and viral load after initiating triple-drug therapy. JAMA 2001; 286 2568–77.
Rates of disease progression by baseline CD4 cell count and viral load after initiating triple-drug therapy.Crossref | GoogleScholarGoogle Scholar | 11722271PubMed |

[83]  Egger M, May M, Chene G, Phillips AN, Ledergerber B, Dabis F, et al Prognosis of HIV-1-infected patients starting highly active antiretroviral therapy: a collaborative analysis of prospective studies. Lancet 2002; 360 119–29.
Prognosis of HIV-1-infected patients starting highly active antiretroviral therapy: a collaborative analysis of prospective studies.Crossref | GoogleScholarGoogle Scholar | 12126821PubMed |

[84]  Palefsky J. Human papillomavirus infection in HIV-infected persons. Top HIV Med 2007; 15 130–3.
| 17720998PubMed |

[85]  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 | 8173899PubMed |

[86]  Koppe DC, Bandeira CB, Rosa MR, Cambruzzi E, Meurer L, Fagundes RB. Prevalence of anal intraepithelial neoplasia in women with genital neoplasia. Dis Colon Rectum 2011; 54 442–5.
Prevalence of anal intraepithelial neoplasia in women with genital neoplasia.Crossref | GoogleScholarGoogle Scholar | 21383564PubMed |

[87]  Calore EE, Giaccio CM, Nadal SR. Prevalence of anal cytological abnormalities in women with positive cervical cytology. Diagn Cytopathol 2011; 39 323–7.
Prevalence of anal cytological abnormalities in women with positive cervical cytology.Crossref | GoogleScholarGoogle Scholar | 21488174PubMed |

[88]  Ferenczy A, Franco EL. Persistent human papillomavirus infection and cervical neoplasia. Lancet Oncol 2002; 3 11–6.
Persistent human papillomavirus infection and cervical neoplasia.Crossref | GoogleScholarGoogle Scholar | 11905599PubMed |

[89]  Fontaine J, Hankins C, Money D, Rachlis A, Pourreaux K, Ferenczy A, et al Human papillomavirus type 16 (HPV-16) viral load and persistence of HPV-16 infection in women infected or at risk for HIV. J Clin Virol 2008; 43 307–12.
Human papillomavirus type 16 (HPV-16) viral load and persistence of HPV-16 infection in women infected or at risk for HIV.Crossref | GoogleScholarGoogle Scholar | 18786854PubMed |

[90]  Lima VD, Hogg RS, Harrigan PR, Moore D, Yip B, Wood E, et al Continued improvement in survival among HIV-infected individuals with newer forms of highly active antiretroviral therapy. AIDS 2007; 21 685–92.
Continued improvement in survival among HIV-infected individuals with newer forms of highly active antiretroviral therapy.Crossref | GoogleScholarGoogle Scholar | 17413689PubMed |

[91]  Cain LE, Cole SR, Chmiel JS, Margolick JB, Rinaldo CRJ, Detels R. Effect of highly active antiretroviral therapy on multiple AIDS-defining illnesses among male HIV seroconverters. Am J Epidemiol 2006; 163 310–5.
Effect of highly active antiretroviral therapy on multiple AIDS-defining illnesses among male HIV seroconverters.Crossref | GoogleScholarGoogle Scholar | 16371516PubMed |

[92]  Engels EA, Biggar RJ, Hall HI, Cross H, Crutchfield A, Finch JL, et al Cancer risk in people infected with human immunodeficiency virus in the United States. Int J Cancer 2008; 123 187–94.
Cancer risk in people infected with human immunodeficiency virus in the United States.Crossref | GoogleScholarGoogle Scholar | 18435450PubMed |

[93]  Clifford GM, Polesel J, Rickenbach M, Dal-Maso L, Keiser O, Kofler A, et al Cancer risk in the Swiss HIV Cohort Study: associations with immunodeficiency, smoking, and highly active antiretroviral therapy. J Natl Cancer Inst 2005; 97 425–32.
Cancer risk in the Swiss HIV Cohort Study: associations with immunodeficiency, smoking, and highly active antiretroviral therapy.Crossref | GoogleScholarGoogle Scholar | 15770006PubMed |

[94]  Partridge JM, Koutsky LA. Genital human papillomavirus infection in men. Lancet Infect Dis 2006; 6 21–31.
Genital human papillomavirus infection in men.Crossref | GoogleScholarGoogle Scholar | 16377531PubMed |

[95]  Heard I, Palefsky JM, Kazatchkine MD. The impact of HIV antiviral therapy on human papillomavirus infections and HPV-related diseases. Antivir Ther 2004; 9 13–22.
| 15040532PubMed |

[96]  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 |

[97]  Palefsky JM, Holly EA, Ralston ML, Da Costa M, Bonner H, Jay N, et al Effect of highly active antiretroviral therapy on the natural history of anal squamous intraepithelial lesions and anal human papillomavirus infection. J Acquir Immune Defic Syndr 2001; 28 422–8.
| 11744829PubMed |

[98]  Aynaud O, Piron D, Barrasso R, Poveda JD. Comparison of clinical, histological, and virological symptoms of HPV in HIV-1 infected men and immunocompetent subjects. Sex Transm Infect 1998; 74 32–4.
Comparison of clinical, histological, and virological symptoms of HPV in HIV-1 infected men and immunocompetent subjects.Crossref | GoogleScholarGoogle Scholar | 9634298PubMed |

[99]  Caliendo AM, St George K, Kao SY, Allega J, Tan BH, LaFontaine R, et al Comparison of quantitative cytomegalovirus (CMV) PCR in plasma and CMV antigenemia assay: clinical utility of the prototype AMPLICOR CMV MONITOR test in transplant recipients. J Clin Microbiol 2000; 38 2122–7.
| 10834964PubMed |

[100]  Lakatosh VP, Boroda AM, Lazarenko LM, Lianenko LO, Dubchak VI, Demchenko SI. The colposcopic characteristics of the pathological processes in the cervix uteri associated with papillomavirus infection. Lik Sprava 1999; 1 67–70. [Ukrainian]
| 10424003PubMed |