Skip to main content
Top
Published in: BMC Infectious Diseases 1/2021

Open Access 01-12-2021 | Human Papillomavirus | Research

Human papillomavirus-associated anal squamous intraepithelial lesions in men who have sex with men and transgender women living with and without HIV in Karachi Pakistan: implications for screening and prevention

Authors: Muslima Ejaz, Muhammad Mubarak, Tazeen Saeed Ali, Sören Andersson, Anna Mia Ekström

Published in: BMC Infectious Diseases | Issue 1/2021

Login to get access

Abstract

Background

Anal squamous intraepithelial lesions (ASIL), strongly related to human papilloma virus (HPV) infection, is more prevalent among men who have sex with men (MSM). However, no such data are available for Pakistan yet, and neither HPV vaccination nor anal-cytology screening is implemented in Pakistan. The purpose of this first ever study was to assess the prevalence of HPV-related anal cytological abnormalities among MSM and transgender women living with and without HIV infection in Pakistan.

Methods

We conducted a cross-sectional study from March 2016 to November 2017 at sexual health centers run by the Perwaaz Trust and the National AIDS Control Program in Karachi. The study enrolled MSM and transgender women aged greater-than-and-equal-to-18-years who reported anal sex in the preceding 6 months. We collected two anal samples for liquid-based cytology and HPV type testing by PCR, and socio-demographic and behavioral data were collected through face-to face interviews. ASIL and its associations with biological and behavioral risk factors were analyzed through Cox regression for prevalence ratios (PR) and corresponding 95% confidence intervals (CIs).

Results

Out of 271 qualifying participants, 79% were MSM and 21% transgender women. The mean age was 28.8 (± 8) years. Almost 35% (93/271) of the study population had ASIL detected, ASIL was significantly more common among participants living with HIV than in HIV negative ((50/118) 42.4%; vs. (43/153) 28.1%) (p ≤ 0.001). Among ASIL, 66% (61/93) had low-grade squamous intraepithelial lesions (LSIL), and 3.6% (3/93) had high-grade squamous intraepithelial lesions (HSIL). The overall, HPV16 positivity was 35.5% (33/93) among all abnormal anal lesions and all 3 HSIL were HPV16 positive, however, HPV16 positivity could show its association with ASIL detection in univariate model only (PRcrude: 2.11(1.39–3.18)). Moreover, any HR-HPV type (PR 3.04; 95% CI 1.75–5.26), concurrent sexually transmitted infection (STI) (2.13; (1.28–3.55)) and HIV + /HPV + coinfection (1.75; (1.07–2.88)) remained independently associated with ASIL in the multivariate model.

Conclusions

Abnormal anal cytology among MSM and transgender is prevalent enough to consider optimal screening regimens. Further studies are required to see if periodic anal cytology can be made part of HIV care and treatment programs among MSM in Pakistan.
Appendix
Available only for authorised users
Literature
1.
go back to reference Lin C, Franceschi S, Clifford GM. Human papillomavirus types from infection to cancer in the anus, according to sex and HIV status: a systematic review and meta-analysis. Lancet Infect Dis. 2018;18(2):198–206.PubMedPubMedCentralCrossRef Lin C, Franceschi S, Clifford GM. Human papillomavirus types from infection to cancer in the anus, according to sex and HIV status: a systematic review and meta-analysis. Lancet Infect Dis. 2018;18(2):198–206.PubMedPubMedCentralCrossRef
2.
go back to reference Islami F, Ferlay J, Lortet-Tieulent J, Bray F, Jemal A. International trends in anal cancer incidence rates. Int J Epidemiol. 2017;46(3):924–38.PubMed Islami F, Ferlay J, Lortet-Tieulent J, Bray F, Jemal A. International trends in anal cancer incidence rates. Int J Epidemiol. 2017;46(3):924–38.PubMed
3.
go back to reference Machalek DA, Poynten M, Jin F, 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(5):487–500.PubMedCrossRef Machalek DA, Poynten M, Jin F, 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(5):487–500.PubMedCrossRef
4.
go back to reference van der Zee RP, Richel O, De Vries H, Prins JM. The increasing incidence of anal cancer: can it be explained by trends in risk groups. Neth J Med. 2013;71(8):401–11.PubMed van der Zee RP, Richel O, De Vries H, Prins JM. The increasing incidence of anal cancer: can it be explained by trends in risk groups. Neth J Med. 2013;71(8):401–11.PubMed
5.
go back to reference Daling JR, Madeleine MM, Johnson LG, et al. Human papillomavirus, smoking, and sexual practices in the etiology of anal cancer. Cancer. 2004;101(2):270–80.PubMedCrossRef Daling JR, Madeleine MM, Johnson LG, et al. Human papillomavirus, smoking, and sexual practices in the etiology of anal cancer. Cancer. 2004;101(2):270–80.PubMedCrossRef
6.
go back to reference Wasserman P, Rubin DS, Turett G. Review: anal intraepithelial neoplasia in HIV-infected men who have sex with men: is screening and treatment justified? AIDS Patient Care STDS. 2017;31(6):245–53.PubMedCrossRef Wasserman P, Rubin DS, Turett G. Review: anal intraepithelial neoplasia in HIV-infected men who have sex with men: is screening and treatment justified? AIDS Patient Care STDS. 2017;31(6):245–53.PubMedCrossRef
7.
go back to reference Nyitray AG, Schick V, Swartz MD, et al. Rationale and design of the prevent anal cancer self-swab study: a protocol for a randomised clinical trial of home-based self-collection of cells for anal cancer screening. BMJ Open. 2021;11(6):e051118.PubMedPubMedCentralCrossRef Nyitray AG, Schick V, Swartz MD, et al. Rationale and design of the prevent anal cancer self-swab study: a protocol for a randomised clinical trial of home-based self-collection of cells for anal cancer screening. BMJ Open. 2021;11(6):e051118.PubMedPubMedCentralCrossRef
8.
go back to reference Clifford GM, Georges D, Shiels MS, et al. A meta-analysis of anal cancer incidence by risk group: toward a unified anal cancer risk scale. Int J Cancer. 2021;148(1):38–47.PubMedCrossRef Clifford GM, Georges D, Shiels MS, et al. A meta-analysis of anal cancer incidence by risk group: toward a unified anal cancer risk scale. Int J Cancer. 2021;148(1):38–47.PubMedCrossRef
9.
go back to reference Colón-López V, Shiels MS, Machin M, et al. Anal cancer risk among people with HIV infection in the United States. J Clin Oncol. 2018;36(1):68.PubMedCrossRef Colón-López V, Shiels MS, Machin M, et al. Anal cancer risk among people with HIV infection in the United States. J Clin Oncol. 2018;36(1):68.PubMedCrossRef
10.
go back to reference Madeleine M, Finch J, Lynch C, Goodman M, Engels E. HPV-related cancers after solid organ transplantation in the United States. Am J Transplant. 2013;13(12):3202–9.PubMedPubMedCentralCrossRef Madeleine M, Finch J, Lynch C, Goodman M, Engels E. HPV-related cancers after solid organ transplantation in the United States. Am J Transplant. 2013;13(12):3202–9.PubMedPubMedCentralCrossRef
11.
go back to reference Gilbert DC, Wakeham K, Langley RE, Vale CL. Increased risk of second cancers at sites associated with HPV after a prior HPV-associated malignancy, a systematic review and meta-analysis. Br J Cancer. 2019;120(2):256–68.PubMedCrossRef Gilbert DC, Wakeham K, Langley RE, Vale CL. Increased risk of second cancers at sites associated with HPV after a prior HPV-associated malignancy, a systematic review and meta-analysis. Br J Cancer. 2019;120(2):256–68.PubMedCrossRef
12.
go back to reference de Martel C, Georges D, Bray F, Ferlay J, Clifford GM. Global burden of cancer attributable to infections in: a worldwide incidence analysis. 2020;8(2):e180–e190. de Martel C, Georges D, Bray F, Ferlay J, Clifford GM. Global burden of cancer attributable to infections in: a worldwide incidence analysis. 2020;8(2):e180–e190.
13.
go back to reference Aldersley J, Lorenz DR, Misra V, Uno H, Gabuzda D. Increased risk of anal squamous cell carcinoma in HIV-positive men with prior hepatitis B virus infection. AIDS. 2019;33(1):145.PubMedCrossRef Aldersley J, Lorenz DR, Misra V, Uno H, Gabuzda D. Increased risk of anal squamous cell carcinoma in HIV-positive men with prior hepatitis B virus infection. AIDS. 2019;33(1):145.PubMedCrossRef
14.
go back to reference Jemal A, Murray T, Samuels A, Ghafoor A, Ward E, Thun MJ. Cancer statistics, 2003. CA Cancer J Clin. 2003;53(1):5–26.PubMedCrossRef Jemal A, Murray T, Samuels A, Ghafoor A, Ward E, Thun MJ. Cancer statistics, 2003. CA Cancer J Clin. 2003;53(1):5–26.PubMedCrossRef
15.
go back to reference Silverberg MJ, Lau B, Justice AC, et al. Risk of anal cancer in HIV-infected and HIV-uninfected individuals in North America. Clin Infect Dis. 2012;54(7):1026–34.PubMedPubMedCentralCrossRef Silverberg MJ, Lau B, Justice AC, et al. Risk of anal cancer in HIV-infected and HIV-uninfected individuals in North America. Clin Infect Dis. 2012;54(7):1026–34.PubMedPubMedCentralCrossRef
16.
go back to reference Deshmukh AA, Suk R, Shiels MS, et al. Recent trends in squamous cell carcinoma of the anus incidence and mortality in the United States, 2001–2015. JNCI J Nat Cancer Inst. 2020;112(8):829–38.PubMedCrossRef Deshmukh AA, Suk R, Shiels MS, et al. Recent trends in squamous cell carcinoma of the anus incidence and mortality in the United States, 2001–2015. JNCI J Nat Cancer Inst. 2020;112(8):829–38.PubMedCrossRef
17.
go back to reference Albuquerque A, Nathan M, Cappello C, Dinis-Ribeiro M. Anal cancer and precancerous lesions: a call for improvement. Lancet Gastroenterol Hepatol. 2021;6(4):327–34.PubMedCrossRef Albuquerque A, Nathan M, Cappello C, Dinis-Ribeiro M. Anal cancer and precancerous lesions: a call for improvement. Lancet Gastroenterol Hepatol. 2021;6(4):327–34.PubMedCrossRef
18.
19.
go back to reference Surawicz CM, Kirby P, Critchlow C, Sayer J, Dunphy C, Kiviat N. Anal dysplasia in homosexual men: role of anoscopy and biopsy. Gastroenterology. 1993;105(3):658–66.PubMedCrossRef Surawicz CM, Kirby P, Critchlow C, Sayer J, Dunphy C, Kiviat N. Anal dysplasia in homosexual men: role of anoscopy and biopsy. Gastroenterology. 1993;105(3):658–66.PubMedCrossRef
20.
go back to reference Frisch M, Olsen JH, Bautz A, Melbye M. Benign anal lesions and the risk of anal cancer. N Engl J Med. 1994;331(5):300–2.PubMedCrossRef Frisch M, Olsen JH, Bautz A, Melbye M. Benign anal lesions and the risk of anal cancer. N Engl J Med. 1994;331(5):300–2.PubMedCrossRef
21.
go back to reference Palefsky JM, Holly EA, Ralston ML, et al. Anal squamous intraepithelial lesions in HIV-positive and HIV-negative homosexual and bisexual men: prevalence and risk factors. JAIDS J Acquir Immune Defic Syndr. 1998;17(4):320–6.CrossRef Palefsky JM, Holly EA, Ralston ML, et al. Anal squamous intraepithelial lesions in HIV-positive and HIV-negative homosexual and bisexual men: prevalence and risk factors. JAIDS J Acquir Immune Defic Syndr. 1998;17(4):320–6.CrossRef
22.
go back to reference Palefsky J. Human papillomavirus-associated malignancies in HIV-positive men and women. Curr Opin Oncol. 1995;7(5):437–41.PubMedCrossRef Palefsky J. Human papillomavirus-associated malignancies in HIV-positive men and women. Curr Opin Oncol. 1995;7(5):437–41.PubMedCrossRef
23.
go back to reference Glynne-Jones R, Nilsson PJ, Aschele C, et al. Anal cancer: ESMO-ESSO-ESTRO clinical practice guidelines for diagnosis, treatment and followup. Ann Oncol. 2014;25(Suppl_3):iii10–20.PubMedCrossRef Glynne-Jones R, Nilsson PJ, Aschele C, et al. Anal cancer: ESMO-ESSO-ESTRO clinical practice guidelines for diagnosis, treatment and followup. Ann Oncol. 2014;25(Suppl_3):iii10–20.PubMedCrossRef
24.
go back to reference Berry JM, Jay N, Cranston RD, et al. Progression of anal high-grade squamous intraepithelial lesions to invasive anal cancer among HIV-infected men who have sex with men. Int J Cancer. 2014;134(5):1147–55.PubMedCrossRef Berry JM, Jay N, Cranston RD, et al. Progression of anal high-grade squamous intraepithelial lesions to invasive anal cancer among HIV-infected men who have sex with men. Int J Cancer. 2014;134(5):1147–55.PubMedCrossRef
25.
go back to reference Palefsky JM, Giuliano AR, Goldstone S, et al. HPV vaccine against anal HPV infection and anal intraepithelial neoplasia. N Engl J Med. 2011;365(17):1576–85.PubMedCrossRef Palefsky JM, Giuliano AR, Goldstone S, et al. HPV vaccine against anal HPV infection and anal intraepithelial neoplasia. N Engl J Med. 2011;365(17):1576–85.PubMedCrossRef
26.
go back to reference Simard EP, Watson M, Saraiya M, Clarke CA, Palefsky JM, Jemal A. Trends in the occurrence of high-grade anal intraepithelial neoplasia in San Francisco: 2000–2009. Cancer. 2013;119(19):3539–45.PubMedCrossRef Simard EP, Watson M, Saraiya M, Clarke CA, Palefsky JM, Jemal A. Trends in the occurrence of high-grade anal intraepithelial neoplasia in San Francisco: 2000–2009. Cancer. 2013;119(19):3539–45.PubMedCrossRef
27.
go back to reference Palefsky JM, Holly EA, Ralston ML, 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(4):320–6.PubMedCrossRef Palefsky JM, Holly EA, Ralston ML, 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(4):320–6.PubMedCrossRef
28.
go back to reference Palefsky JM, Holly EA, Efirdc JT, et al. Anal intraepithelial neoplasia in the highly active antiretroviral therapy era among HIV-positive men who have sex with men. AIDS. 2005;19(13):1407–14.PubMedCrossRef Palefsky JM, Holly EA, Efirdc JT, et al. Anal intraepithelial neoplasia in the highly active antiretroviral therapy era among HIV-positive men who have sex with men. AIDS. 2005;19(13):1407–14.PubMedCrossRef
29.
go back to reference Ong JJ, Chen M, Grulich AE, Fairley CK. Regional and national guideline recommendations for digital ano-rectal examination as a means for anal cancer screening in HIV positive men who have sex with men: a systematic review. BMC Cancer. 2014;14(1):1–7.CrossRef Ong JJ, Chen M, Grulich AE, Fairley CK. Regional and national guideline recommendations for digital ano-rectal examination as a means for anal cancer screening in HIV positive men who have sex with men: a systematic review. BMC Cancer. 2014;14(1):1–7.CrossRef
30.
go back to reference 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(8):634–41.PubMedCrossRef 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(8):634–41.PubMedCrossRef
31.
go back to reference Oon SF, Winter DC. Perianal condylomas, anal squamous intraepithelial neoplasms and screening: a review of the literature. J Med Screen. 2010;17(1):44–9.PubMedCrossRef Oon SF, Winter DC. Perianal condylomas, anal squamous intraepithelial neoplasms and screening: a review of the literature. J Med Screen. 2010;17(1):44–9.PubMedCrossRef
32.
go back to reference Chiao EY, Giordano TP, Palefsky JM, Tyring S, Serag HE. Screening HIV-infected individuals for anal cancer precursor lesions: a systematic review. Clin Infect Dis. 2006;43(2):223–33.PubMedCrossRef Chiao EY, Giordano TP, Palefsky JM, Tyring S, Serag HE. Screening HIV-infected individuals for anal cancer precursor lesions: a systematic review. Clin Infect Dis. 2006;43(2):223–33.PubMedCrossRef
33.
go back to reference Ong JJ, Fairley CK, Carroll S, et al. Cost-effectiveness of screening for anal cancer using regular digital ano-rectal examinations in men who have sex with men living with HIV. J Int AIDS Soc. 2016;19(1):20514.PubMedPubMedCentralCrossRef Ong JJ, Fairley CK, Carroll S, et al. Cost-effectiveness of screening for anal cancer using regular digital ano-rectal examinations in men who have sex with men living with HIV. J Int AIDS Soc. 2016;19(1):20514.PubMedPubMedCentralCrossRef
34.
go back to reference 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(5):415–22.PubMedCrossRef 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(5):415–22.PubMedCrossRef
35.
go back to reference Cranston RD, Hart SD, Gornbein JA, Hirschowitz SL, Cortina G, Moe AA. The prevalence, and predictive value, of abnormal anal cytology to diagnose anal dysplasia in a population of HIV-positive men who have sex with men. Int J STD AIDS. 2007;18(2):77–80.PubMedCrossRef Cranston RD, Hart SD, Gornbein JA, Hirschowitz SL, Cortina G, Moe AA. The prevalence, and predictive value, of abnormal anal cytology to diagnose anal dysplasia in a population of HIV-positive men who have sex with men. Int J STD AIDS. 2007;18(2):77–80.PubMedCrossRef
36.
go back to reference Chin-Hong PV, Vittinghoff E, Cranston RD, et al. Age-related prevalence of anal cancer precursors in homosexual men: the EXPLORE study. J Natl Cancer Inst. 2005;97(12):896–905.PubMedCrossRef Chin-Hong PV, Vittinghoff E, Cranston RD, et al. Age-related prevalence of anal cancer precursors in homosexual men: the EXPLORE study. J Natl Cancer Inst. 2005;97(12):896–905.PubMedCrossRef
37.
go back to reference Hillman RJ, van Leeuwen MT, Vajdic CM, et al. Prevalence and predictors of high-grade anal intraepithelial neoplasia in a community-based sample of homosexual men. Sex Health. 2012;9(6):574–9.PubMedCrossRef Hillman RJ, van Leeuwen MT, Vajdic CM, et al. Prevalence and predictors of high-grade anal intraepithelial neoplasia in a community-based sample of homosexual men. Sex Health. 2012;9(6):574–9.PubMedCrossRef
38.
go back to reference Gaisa M, Sigel K, Hand J, Goldstone S. High rates of anal dysplasia in HIV-infected men who have sex with men, women, and heterosexual men. AIDS. 2014;28(2):215–22.PubMedCrossRef Gaisa M, Sigel K, Hand J, Goldstone S. High rates of anal dysplasia in HIV-infected men who have sex with men, women, and heterosexual men. AIDS. 2014;28(2):215–22.PubMedCrossRef
39.
go back to reference Solomon D, Davey D, Kurman R, et al. The 2001 Bethesda System: terminology for reporting results of cervical cytology. JAMA. 2002;287(16):2114–9.PubMedCrossRef Solomon D, Davey D, Kurman R, et al. The 2001 Bethesda System: terminology for reporting results of cervical cytology. JAMA. 2002;287(16):2114–9.PubMedCrossRef
40.
go back to reference Ruanpeng D, Chariyalertsak S, Kaewpoowat Q, et al. Cytological anal squamous intraepithelial lesions associated with anal high-risk human papillomavirus infections among men who have sex with men in Northern Thailand. PLoS ONE. 2016;11(5):e0156280.PubMedPubMedCentralCrossRef Ruanpeng D, Chariyalertsak S, Kaewpoowat Q, et al. Cytological anal squamous intraepithelial lesions associated with anal high-risk human papillomavirus infections among men who have sex with men in Northern Thailand. PLoS ONE. 2016;11(5):e0156280.PubMedPubMedCentralCrossRef
41.
go back to reference Yang Y, Li X, Zhang Z, et al. Association of human papillomavirus infection and abnormal anal cytology among HIV-infected MSM in Beijing, China. PLoS ONE. 2012;7(4):e35983.PubMedPubMedCentralCrossRef Yang Y, Li X, Zhang Z, et al. Association of human papillomavirus infection and abnormal anal cytology among HIV-infected MSM in Beijing, China. PLoS ONE. 2012;7(4):e35983.PubMedPubMedCentralCrossRef
42.
go back to reference Cheng SH, Chu FY, Wang CC, Hsueh YM. Screening and risk factors for anal cancer precursors in men infected with HIV in Taiwan. J Med Virol. 2014;86(2):193–201.PubMedCrossRef Cheng SH, Chu FY, Wang CC, Hsueh YM. Screening and risk factors for anal cancer precursors in men infected with HIV in Taiwan. J Med Virol. 2014;86(2):193–201.PubMedCrossRef
43.
go back to reference Piketty C, Darragh TM, Heard I, 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(2):96–9.PubMedCrossRef Piketty C, Darragh TM, Heard I, 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(2):96–9.PubMedCrossRef
44.
go back to reference 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(9):1685–91.PubMedCrossRef 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(9):1685–91.PubMedCrossRef
45.
go back to reference 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(7):1011–6.PubMedCrossRef 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(7):1011–6.PubMedCrossRef
46.
go back to reference Anderson J, Hoy J, Hillman R, et al. Abnormal anal cytology in high-risk human papilloma virus infection in HIV-infected Australians. Sex Transm Infect. 2008;84(2):94–6.PubMedCrossRef Anderson J, Hoy J, Hillman R, et al. Abnormal anal cytology in high-risk human papilloma virus infection in HIV-infected Australians. Sex Transm Infect. 2008;84(2):94–6.PubMedCrossRef
47.
go back to reference Arora R, Pandhi D, Mishra K, Bhattacharya SN, Yhome VA. Anal cytology and p16 immunostaining for screening anal intraepithelial neoplasia in HIV-positive and HIV-negative men who have sex with men: a cross-sectional study. Int J STD AIDS. 2014;25(10):726–33.PubMedCrossRef Arora R, Pandhi D, Mishra K, Bhattacharya SN, Yhome VA. Anal cytology and p16 immunostaining for screening anal intraepithelial neoplasia in HIV-positive and HIV-negative men who have sex with men: a cross-sectional study. Int J STD AIDS. 2014;25(10):726–33.PubMedCrossRef
48.
go back to reference Palefsky JM, Holly EA, Hogeboom CJ, 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 Hum Retrovirol. 1998;17(4):314–9.PubMedCrossRef Palefsky JM, Holly EA, Hogeboom CJ, 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 Hum Retrovirol. 1998;17(4):314–9.PubMedCrossRef
49.
go back to reference 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(11):843–9.PubMedCrossRef 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(11):843–9.PubMedCrossRef
50.
go back to reference 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(2):126–33.PubMedPubMedCentralCrossRef 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(2):126–33.PubMedPubMedCentralCrossRef
51.
go back to reference Goldstone SE, Lowe B, Rothmann T, Nazarenko I. Evaluation of the hybrid capture 2 assay for detecting anal high-grade dysplasia. Int J Cancer. 2012;131(7):1641–8.PubMedCrossRef Goldstone SE, Lowe B, Rothmann T, Nazarenko I. Evaluation of the hybrid capture 2 assay for detecting anal high-grade dysplasia. Int J Cancer. 2012;131(7):1641–8.PubMedCrossRef
52.
go back to reference Critchlow CW, Surawicz CM, Holmes KK, 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(11):1255–62.PubMedCrossRef Critchlow CW, Surawicz CM, Holmes KK, 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(11):1255–62.PubMedCrossRef
53.
go back to reference 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(12):1258–65.PubMedCrossRef 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(12):1258–65.PubMedCrossRef
54.
go back to reference 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(7):1626–36.PubMedCrossRef 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(7):1626–36.PubMedCrossRef
55.
go back to reference Salit IE, Tinmouth J, Chong S, 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(7):1986–92.PubMedCrossRef Salit IE, Tinmouth J, Chong S, 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(7):1986–92.PubMedCrossRef
56.
go back to reference de Pokomandy A, Rouleau D, Ghattas G, 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(9):1174–81.PubMedCrossRef de Pokomandy A, Rouleau D, Ghattas G, 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(9):1174–81.PubMedCrossRef
57.
go back to reference 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(5):495–503.PubMedCrossRef 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(5):495–503.PubMedCrossRef
58.
go back to reference Friedman HB, Saah AJ, Sherman ME, et al. Human papillomavirus, anal squamous intraepithelial lesions, and human immunodeficiency virus in a cohort of gay men. J Infect Dis. 1998;178(1):45–52.PubMedCrossRef Friedman HB, Saah AJ, Sherman ME, et al. Human papillomavirus, anal squamous intraepithelial lesions, and human immunodeficiency virus in a cohort of gay men. J Infect Dis. 1998;178(1):45–52.PubMedCrossRef
59.
go back to reference 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(2):361–7.PubMedCrossRef 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(2):361–7.PubMedCrossRef
60.
go back to reference Vajdic CM, van Leeuwen MT, Jin F, et al. Anal human papillomavirus genotype diversity and co-infection in a community-based sample of homosexual men. Sex Transm Infect. 2009;85(5):330–5.PubMedCrossRef Vajdic CM, van Leeuwen MT, Jin F, et al. Anal human papillomavirus genotype diversity and co-infection in a community-based sample of homosexual men. Sex Transm Infect. 2009;85(5):330–5.PubMedCrossRef
61.
go back to reference Prestage G, Mao L, Fogarty A, 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(6):530–5.PubMedCrossRef Prestage G, Mao L, Fogarty A, 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(6):530–5.PubMedCrossRef
62.
go back to reference Limia CM, Soto Y, Garcia Y, et al. Human papillomavirus infection in anal intraepithelial lesions from HIV infected Cuban men. Infect Agent Cancer. 2017;12(1):1–8.CrossRef Limia CM, Soto Y, Garcia Y, et al. Human papillomavirus infection in anal intraepithelial lesions from HIV infected Cuban men. Infect Agent Cancer. 2017;12(1):1–8.CrossRef
63.
go back to reference Schlecht HP, Fugelso DK, Murphy RK, et al. Frequency of occult high-grade squamous intraepithelial neoplasia and invasive cancer within anal condylomata in men who have sex with men. Clin Infect Dis. 2010;51(1):107–10.PubMedCrossRef Schlecht HP, Fugelso DK, Murphy RK, et al. Frequency of occult high-grade squamous intraepithelial neoplasia and invasive cancer within anal condylomata in men who have sex with men. Clin Infect Dis. 2010;51(1):107–10.PubMedCrossRef
64.
go back to reference Goldstone S, Palefsky JM, Giuliano AR, 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(1):66–74.PubMedPubMedCentralCrossRef Goldstone S, Palefsky JM, Giuliano AR, 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(1):66–74.PubMedPubMedCentralCrossRef
65.
go back to reference Conley L, Bush T, Darragh TM, 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(10):1567–76.PubMedCrossRef Conley L, Bush T, Darragh TM, 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(10):1567–76.PubMedCrossRef
66.
go back to reference Dona MG, Benevolo M, Vocaturo A, et al. Anal cytological abnormalities and epidemiological correlates among men who have sex with men at risk for HIV-1 infection. BMC Cancer. 2012;12:476.PubMedPubMedCentralCrossRef Dona MG, Benevolo M, Vocaturo A, et al. Anal cytological abnormalities and epidemiological correlates among men who have sex with men at risk for HIV-1 infection. BMC Cancer. 2012;12:476.PubMedPubMedCentralCrossRef
67.
go back to reference Nyitray A, Nielson CM, Harris RB, et al. Prevalence of and risk factors for anal human papillomavirus infection in heterosexual men. J Infect Dis. 2008;197(12):1676–84.PubMedCrossRef Nyitray A, Nielson CM, Harris RB, et al. Prevalence of and risk factors for anal human papillomavirus infection in heterosexual men. J Infect Dis. 2008;197(12):1676–84.PubMedCrossRef
68.
go back to reference Piketty C, Darragh TM, Da Costa M, 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(6):453–9.PubMedCrossRef Piketty C, Darragh TM, Da Costa M, 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(6):453–9.PubMedCrossRef
69.
go back to reference Darragh TM, Tokugawa D, Castle PE, et al. Interrater agreement of anal cytology. Cancer Cytopathol. 2013;121(2):72–8.PubMedCrossRef Darragh TM, Tokugawa D, Castle PE, et al. Interrater agreement of anal cytology. Cancer Cytopathol. 2013;121(2):72–8.PubMedCrossRef
70.
go back to reference Clarke MA, Cheung LC, Lorey T, et al. 5-year prospective evaluation of cytology, human papillomavirus testing, and biomarkers for detection of anal precancer in human immunodeficiency virus-positive men who have sex with men. Clin Infect Dis. 2019;69(4):631–8.PubMedCrossRef Clarke MA, Cheung LC, Lorey T, et al. 5-year prospective evaluation of cytology, human papillomavirus testing, and biomarkers for detection of anal precancer in human immunodeficiency virus-positive men who have sex with men. Clin Infect Dis. 2019;69(4):631–8.PubMedCrossRef
71.
go back to reference 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(9):1127–34.PubMedCrossRef 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(9):1127–34.PubMedCrossRef
72.
go back to reference Chin-Hong PV, Berry JM, Cheng SC, 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(5):300–6.PubMedCrossRef Chin-Hong PV, Berry JM, Cheng SC, 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(5):300–6.PubMedCrossRef
73.
go back to reference Blaser N, Bertisch B, Kouyos RD, et al. Impact of screening and antiretroviral therapy on anal cancer incidence in HIV-positive MSM. AIDS. 2017;31(13):1859–66.PubMedCrossRef Blaser N, Bertisch B, Kouyos RD, et al. Impact of screening and antiretroviral therapy on anal cancer incidence in HIV-positive MSM. AIDS. 2017;31(13):1859–66.PubMedCrossRef
Metadata
Title
Human papillomavirus-associated anal squamous intraepithelial lesions in men who have sex with men and transgender women living with and without HIV in Karachi Pakistan: implications for screening and prevention
Authors
Muslima Ejaz
Muhammad Mubarak
Tazeen Saeed Ali
Sören Andersson
Anna Mia Ekström
Publication date
01-12-2021

Other articles of this Issue 1/2021

BMC Infectious Diseases 1/2021 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.