Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

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.
ADVANCED SEARCH
Log in
Top
BMC Public Health
Published in: BMC Public Health 3/2017

Open Access 01-07-2017 | Research

Prevalence of anogenital HPV infection, related disease and risk factors among HIV-infected men in inner-city Johannesburg, South Africa: baseline findings from a cohort study

Authors: Admire Chikandiwa, Lucy Chimoyi, Pedro T Pisa, Matthew F Chersich, Etienne E Muller, Pamela Michelow, Philippe Mayaud, Sinead Delany-Moretlwe

Published in: BMC Public Health | Special Issue 3/2017

Login to get access

Abstract

Background

Persistent high-risk human papillomavirus (HR-HPV) infection is associated with the development of anogenital cancers, particularly in men living with HIV (MLWH). We describe the prevalence of anogenital HPV infection, abnormal anal cytology and anogenital warts (AGWs) in MLWH in Johannesburg, and explore whether HPV infection and receipt of antiretroviral treatment is associated with detection of abnormal anal cytology and AGWs.

Methods

We enrolled a cohort of 304 sexually-active MLWH ≥18 years, who completed a questionnaire and physical examination. Genital swabs were collected from all men and intra-anal swabs from 250 (82%). Swabs were tested for HPV DNA and genotypes, and anal smears graded using the Bethesda classification. Factors associated with anogenital disease were assessed by logistic regression models.

Results

Two thirds were receiving antiretroviral treatment, for a median 33 months (IQR = 15–58) and 54% were HIV-virologically suppressed. Only 5% reported ever having sex with men. Among 283 genital swabs with valid results, 79% had any HPV, 52% had HR-HPV and 27% had >1 HR-HPV infection. By comparison, 39% of the 227 valid intra-anal swabs had detectable HPV, 25% had any HR-HPV and 7% >1 HR infection. While most anal smears were normal (51%), 20% had ASCUS and 29% were LSIL. No cases had HSIL or cancer. Infection with >1 HR type (adjusted OR [aOR] = 2.39; 95%CI = 1.02–5.58) and alpha-9 types (aOR = 3.98; 95%CI = 1.42–11.16) were associated with having abnormal cytology. Prevalence of AGWs was 12%. Infection with any LR type (aOR = 41.28; 95%CI = 13.57–125.62), >1 LR type (aOR = 4.14; 95%CI = 1.60–10.69), being <6 months on antiretroviral treatment (aOR = 6.90; 95%CI = 1.63–29.20) and having a CD4+ count <200 cells/μL (aOR = 5.48; 95%CI: 1.60–18.78) were associated with having AGWs.

Conclusions

In this population, anogenital HR-HPV infection and associated low-grade disease is common, but severe anal dysplasia was not detected. Findings reinforce the need for HPV vaccination in men for preventing both AGWs and HR-HPV infection. Given the absence of anal HSILs, however, the findings do not support the use of anal screening programmes in this population.
Appendix
Available only for authorised users
Literature
1.
Gross G, Pfister H. Role of human papillomavirus in penile cancer, penile intraepithelial squamous cell neoplasias and in genital warts. Med Microbiol Immun. 2004;193:35–44.CrossRef
2.
Delany-Moretlwe S, Chikandiwa A, Gibbs J. Human papillomavirus infection and disease in men: impact of HIV. Southern African J HIV Med. 2013;14(4):183–8.CrossRef
3.
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(6):540–52.CrossRefPubMed
4.
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.CrossRefPubMed
5.
Moscicki A-B, Schiffman M, Burchell A, Albero G, Giuliano A, Goodman MT, Kjaer SK, Palefsky J. Updating the natural history of human papillomavirus and anogenital cancers. Vaccine. 2012;30(0 5):F24–33.CrossRefPubMedPubMedCentral
6.
Machalek DA, Poynten M, Jin F, Fairley CK, Farnsworth A, Garland SM, Hillman RJ, Petoumenos K, Roberts J, Tabrizi SN, 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.CrossRefPubMed
7.
De Vuyst H, Clifford G, Li N, Franceschi S. HPV infection in Europe. Eur J Cancer. 2009;45(15):2632–9.CrossRefPubMed
8.
Forman D, de Martel C, Lacey CJ, Soerjomataram I, Lortet-Tieulent J, Bruni L, Vignat J, Ferlay J, Bray F, Plummer M, et al. Global burden of human papillomavirus and related diseases. Vaccine. 2012;20(30):055.
9.
Dunne EF, Nielson CM, Stone KM, Markowitz LE, Giuliano AR. Prevalence of HPV infection among men: a systematic review of the literature. J Infect Dis. 2006;194(8):1044–57.CrossRefPubMed
10.
de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H. Classification of papillomaviruses. Virology. 2004;324(1):17–27.CrossRefPubMed
11.
Jeynes C, Chung MC. Challenor R: 'Shame on you'--the psychosocial impact of genital warts. Int J STD AIDS. 2009;20(8):557–60.CrossRefPubMed
12.
Wiley DJ, Douglas J, Beutner K, Cox T, Fife K, Moscicki AB, Fukumoto L. External genital warts: diagnosis, treatment, and prevention. Clin Infect Dis. 2002;35(Suppl 2):S210–24.CrossRefPubMed
13.
Insinga RP, Dasbach EJ, Elbasha EH. Assessing the annual economic burden of preventing and treating anogenital human papillomavirus-related disease in the US: analytic framework and review of the literature. PharmacoEconomics. 2005;23(11):1107–22.CrossRefPubMed
14.
Ng'ayo MO, Bukusi E, Rowhani-Rahbar A, Koutsky LA, Feng Q, Kwena ZA, Holmes KK. Epidemiology of human papillomavirus infection among fishermen along Lake Victoria shore in the Kisumu District, Kenya. Sex Transm Infect. 2008;84(1):62–6.CrossRefPubMed
15.
Auvert B, Sobngwi-Tambekou J, Cutler E, Nieuwoudt M, Lissouba P, Puren A, Taljaard D. Effect of male circumcision on the prevalence of high-risk human papillomavirus in young men: results of a randomized controlled trial conducted in Orange farm, South Africa. J Infect Dis. 2009;199(1):14–9.CrossRefPubMedPubMedCentral
16.
Smith JS, Moses S, Hudgens M, Parker CB, Maclean I, Ndinya-achola JO, Snijders PJF, Chris JLM, Bailey RC. Increased risk of HIV acquisition among Kenyan men with human papillomavirus infection. J Infect Dis. 2010;201:1677–85.CrossRefPubMedPubMedCentral
17.
Müller EE, Chirwa TF, Da L. Human papillomavirus (HPV) infection in heterosexual South African men attending sexual health services: associations between HPV and HIV serostatus. Sex Transm Infect. 2010;86:175–80.CrossRefPubMed
18.
Veldhuijzen NJ, Dhont N, Vyankandondera J, Gasarabwe A, Busasa R, Crucitti T, van de Wijgert JH. Prevalence and concordance of HPV, HIV, and HSV-2 in heterosexual couples in Kigali, Rwanda. Sex Transm Dis. 2012;39(2):128–35.CrossRefPubMed
19.
Olesen TB, Iftner T, Mwaiselage J, Kahesa C, Rasch V, Ngoma T, Munk C, Kjaer SK. Prevalence and type distribution of human papillomavirus among 1813 men in Tanzania and the relationship to HIV status. Sex Transm Dis. 2013;40(7):592–8.CrossRefPubMed
20.
Mbulawa ZZ, Marais DJ, Johnson LF, Coetzee D, Williamson AL. Impact of human immunodeficiency virus on the natural history of human papillomavirus genital infection in South African men and women. J Infect Dis. 2012;206
21.
Tobian AAR, Kigozi G, Gravitt PE, Xiao C, Serwadda D, Eaton KP, Kong X, Wawer MJ, Nalugoda F, Quinn TC, et al. Human papillomavirus incidence and clearance among HIV-positive and HIV-negative men in Rakai, Uganda. AIDS (London, England). 2012;26(12):1555–65.CrossRef
22.
Backes DM, Snijders PJ, Hudgens MG, Bailey RC, Bogaarts M, Agot K, Agingu W, Moses S, Meijer CJ, Smith JS. Sexual behaviour and less frequent bathing are associated with higher human papillomavirus incidence in a cohort study of uncircumcised Kenyan men. Sex Transm Infect. 2013;89(2):148–55.CrossRefPubMed
23.
Shiels MS, Pfeiffer RM, Gail MH, Hall HI, Li J, Chaturvedi AK, Bhatia K, Uldrick TS, Yarchoan R, Goedert JJ, et al. Cancer burden in the HIV-infected population in the United States. J Natl Cancer Inst. 2011;103(9):753–62.CrossRefPubMedPubMedCentral
24.
Nyitray AG, Smith D, Villa L, Lazcano-Ponce E, Abrahamsen M, Papenfuss M, Giuliano AR. Prevalence of and risk factors for anal human papillomavirus infection in men who have sex with women: a cross-national study. J Infect Dis. 2010;201(10):1498–508.CrossRefPubMedPubMedCentral
25.
Beachler DC, Weber KM, Margolick JB, Strickler HD, Cranston RD, Burk RD, Wiley DJ, Minkoff H, Reddy S, Stammer EE, et al. Risk factors for oral HPV infection among a high prevalence population of HIV-positive and at-risk HIV-negative adults. Cancer Epidemiol Biomarkers Prev. 2012;21(1):122–33.CrossRefPubMed
26.
Silverberg MJ, Ahdieh L, Munoz A, Anastos K, Burk RD, Cu-Uvin S, Duerr A, Greenblatt RM, Klein RS, Massad S, et al. The impact of HIV infection and immunodeficiency on human papillomavirus type 6 or 11 infection and on genital warts. Sex Transm Dis. 2002;29(8):427–35.CrossRefPubMed
27.
Neme S, Wahome E, Mwashigadi G, Thiong'o AN, Stekler JD, Wald A, Sanders EJ, Graham SM. Prevalence, incidence, and clearance of Anogenital warts in Kenyan men reporting high-risk sexual behavior, including men who have sex with men. Open Forum Infect Dis. 2015;2(2):ofv070.CrossRefPubMedPubMedCentral
28.
Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol. 2011;29:235–71.CrossRefPubMed
29.
Piketty C, Cochand-Priollet B, Lanoy E, Si-Mohamed A, Trabelsi S, Tubiana R, Girard PM, Weiss L, Costagliola D. Lack of regression of anal squamous intraepithelial lesions despite immune restoration under cART. AIDS. 2013;27(3):401–6.CrossRefPubMed
30.
Borghetti A, Cattani P, Maria G, D'Onghia S, Santangelo R, Marchetti S, Farina S, Cauda R, De Luca A, Di Giambenedetto S. Prevalence, incidence and predictors of anal high-risk HPV infections and cytological abnormalities in HIV-infected individuals. J Inf Secur. 2015;70(1):60–71.
31.
Giuliano ARPJ, Goldstone S, Moreira ED Jr, Penny ME, Aranda C, et al. Efficacy of quadrivalent HPV vaccine against HPV infection and disease in males. N Engl J Med. 2011;364:401–11.CrossRefPubMedPubMedCentral
32.
Ali H, Donovan B, Wand H, Read TR, Regan DG, Grulich AE, Fairley CK, Guy RJ. Genital warts in young Australians five years into national human papillomavirus vaccination programme: national surveillance data. BMJ. 2013;346:f2032.CrossRefPubMed
33.
Simbayi L, Shisana O, Rehle T, Onoya D, Jooste S, Zungu N, Zuma K. South African national HIV prevalence, incidence and behaviour survey, 2012. Pretoria: Human Sciences Research Council; 2014.
34.
35.
Weaver BA, Feng Q, Holmes KK, Kiviat N, Lee SK, Meyer C, Stern M, Koutsky LA. Evaluation of genital sites and sampling techniques for detection of human papillomavirus DNA in men. J Infect Dis. 2004;189(4):677–85.CrossRefPubMed
36.
37.
Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, Cogliano V, on behalf of the WHO International Agency for Research on Cancer Monograph Working Group. A review of human carcinogens—part B: biological agents. Lancet Oncol. 2009;10:321–2.CrossRefPubMed
38.
Solomon D. The Bethesda System for Reporting Cervical Cytology: Definitions, Criteria, and Explanatory Notes. 2nd edition. Edited by Nayar R, Wilbur D. Geneva: Springer; 2001.
39.
Ingles DJ, Lin H-Y, Fulp WJ, Sudenga SL, Lu B, Schabath MB, Papenfuss MR, Abrahamsen ME, Salmeron J, Villa LL, et al. An analysis of HPV infection incidence and clearance by genotype and age in men: the HPV infection in men (HIM) study. Papillomavirus Res. 2015;1:126–35.CrossRefPubMedPubMedCentral
40.
Colón-López V, Ortiz AP, Del Toro-Mejías L, Clatts MC, Palefsky JM. Epidemiology of anal HPV infection in high-risk men attending a sexually transmitted infection Clinic in Puerto Rico. PLoS One. 2014;9(1):e83209.CrossRefPubMedPubMedCentral
41.
StataCorp: Stata statistical software, release 12. College Station, TX: StataCorp LP; 2012.
42.
Mbulawa ZZA, Coetzee D, Williamson A-L. Human papillomavirus prevalence in South African women and men according to age and human immunodeficiency virus status. BMC Infect Dis. 2015;15(1):1–11.CrossRef
43.
Piketty C, Darragh TM, Costa MD, Bruneval P, Heard I, Kazatchkine MD, Palefsky JM. 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.CrossRefPubMed
44.
Conley L, Bush T, Darragh TM, Palefsky JM, Unger ER, Patel P, Kojic EM, Cu-Uvin S, Martin H, Overton ET, 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.CrossRefPubMed
45.
Lee CH, Lee SH, Lee S, Cho H, Kim K-H, Lee JE. Jung EJ, lee Sj, Kim EJ, Kim KH et al: anal human Papillomavirus infection among HIV-infected men in Korea. PLoS One. 2016;11(8):e0161460.CrossRefPubMedPubMedCentral
46.
Nyitray AG. The epidemiology of anal human papillomavirus infection among women and men having sex with women. Sex Health. 2012;9(6):538–46.CrossRefPubMed
47.
Hernandez BY, Wilkens LR, Zhu X, Thompson P, McDuffie K, Shvetsov YB, Kamemoto LE, Killeen J, Ning L, Goodman MT. Transmission of human Papillomavirus in heterosexual couples. Emerg Infect Dis. 2008;14(6):888–94.CrossRefPubMedPubMedCentral
48.
Ferenczy A, Bergeron C, Richart RM. Human papillomavirus DNA in fomites on objects used for the management of patients with genital human papillomavirus infections. Obstet Gynecol. 1989;74(6):950–4.PubMed
49.
Partridge JM, Hughes JP, Feng Q, Winer RL, Weaver BA, Xi LF, Stern ME, Lee SK, O'Reilly SF, Hawes SE, et al. Genital human papillomavirus infection in men: incidence and risk factors in a cohort of university students. J Infect Dis. 2007;196(8):1128–36.CrossRefPubMed
50.
Kines RC, Thompson CD, Lowy DR, Schiller JT, Day PM. The initial steps leading to papillomavirus infection occur on the basement membrane prior to cell surface binding. Proc Natl Acad Sci U S A. 2009;106(48):20458–63.CrossRefPubMedPubMedCentral
51.
Torres M, Gonzalez C, del Romero J, Viciana P, Ocampo A, Rodriguez-Fortunez P, Masia M, Blanco JR, Portilla J, Rodriguez C, et al. Anal human papillomavirus genotype distribution in HIV-infected men who have sex with men by geographical origin, age, and cytological status in a Spanish cohort. J Clin Microbiol. 2013;51(11):3512–20.CrossRefPubMedPubMedCentral
52.
Darwich L, Canadas MP, Videla S, Coll J, Pinol M, Cobarsi P, Molina-Lopez RA, Vela S, Garcia-Cuyas F, Llatjos M, et al. Condylomata, cytological abnormalities and human papillomavirus infection in the anal canal in HIV-infected men. HIV Med. 2012;13(9):549–57.CrossRefPubMed
53.
Banura C, Mirembe FM, Orem J, Mbonye AK, Kasasa S, Mbidde EK. Prevalence, incidence and risk factors for anogenital warts in sub Saharan Africa: a systematic review and meta analysis. Infect Agent Cancer. 2013;8(1):27.CrossRefPubMedPubMedCentral
54.
Poynten IM, Waterboer T, Jin F, Templeton DJ, Prestage G, Donovan B, Pawlita M, Fairley CK, Garland SM, Grulich AE. Human papillomavirus types 6 and 11 seropositivity: risk factors and association with ano-genital warts among homosexual men. J Inf Secur. 2013;66(6):503–11.
55.
Kojic EM, Kang M, Cespedes MS, Umbleja T, Godfrey C, Allen RT, Firnhaber C, Grinsztejn B, Palefsky JM, Webster-Cyriaque JY, et al. Immunogenicity and safety of the Quadrivalent human Papillomavirus vaccine in HIV-1–infected women. Clin Infect Dis. 2014;59(1):127–35.CrossRefPubMedPubMedCentral
56.
Fife KH, Wu JW, Squires KE, Watts DH, Andersen JW, Brown DR. Prevalence and persistence of cervical human Papillomavirus infection in HIV-positive women initiating highly-active antiretroviral therapy. J Acquir Immune Defic Syndr. 2009;51(3, 274):–282.
57.
Deshmukh AA, Chhatwal J, Chiao EY, Nyitray AG, Das P, Cantor SB. Long-Term Outcomes of Adding HPV Vaccine to the Anal Intraepithelial Neoplasia Treatment Regimen in HIV-Positive Men Who Have Sex with Men. Clinical Infectious Diseases. 2015;61(10):1527-35.
58.
Swedish KA, Factor SH, Goldstone SE. Prevention of recurrent high-grade anal neoplasia with quadrivalent human papillomavirus vaccination of men who have sex with men: a nonconcurrent cohort study. Clin Infect Dis. 2012;54(7):891–8.CrossRefPubMed
59.
Swedish KA, Goldstone SE. Prevention of anal Condyloma with Quadrivalent human Papillomavirus vaccination of older men who have sex with men. PLoS One. 2014;9(4):e93393.CrossRefPubMedPubMedCentral
60.
Low AJ, Clayton T, Konate I, Nagot N, Ouedraogo A, Huet C, Didelot-Rousseau M-N, Segondy M, Van de Perre P, Mayaud P: Genital warts and infection with human immunodeficiency virus in high-risk women in Burkina Faso: a longitudinal study. BMC Infect Dis 2011, 11(1):1-9.
61.
62.
Abramowitz L, Benabderrahmane D, Ravaud P, Walker F, Rioux C, Jestin C, Bouvet E, Soule JC, Leport C, Duval X. Anal squamous intraepithelial lesions and condyloma in HIV-infected heterosexual men, homosexual men and women: prevalence and associated factors. AIDS. 2007;21(11):1457–65.CrossRefPubMed
63.
Steinau M, Onyekwuluje JM, Scarbrough MZ, Unger ER, Dillner J, Zhou T. Performance of commercial reverse line blot assays for human Papillomavirus genotyping. J Clin Microbiol. 2012;50(5):1539–44.CrossRefPubMedPubMedCentral
Metadata
Title
Prevalence of anogenital HPV infection, related disease and risk factors among HIV-infected men in inner-city Johannesburg, South Africa: baseline findings from a cohort study
Authors
Admire Chikandiwa
Lucy Chimoyi
Pedro T Pisa
Matthew F Chersich
Etienne E Muller
Pamela Michelow
Philippe Mayaud
Sinead Delany-Moretlwe
Publication date
01-07-2017
Publisher
BioMed Central
Published in
BMC Public Health / Issue Special Issue 3/2017
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/s12889-017-4354-0

Other articles of this Special Issue 3/2017

BMC Public Health 3/2017 Go to the issue

Research

Sexual and reproductive health outcomes among female sex workers in Johannesburg and Pretoria, South Africa: Recommendations for public health programmes

Research

Intersections between polyvictimisation and mental health among adolescents in five urban disadvantaged settings: the role of gender

Introduction

At the Heart of the Problem: Health in Johannesburg’s Inner-City

Research

Using surrogate vaccines to assess feasibility and acceptability of future HIV vaccine trials in men: a randomised trial in inner-city Johannesburg, South Africa

Commentary

Analysing local-level responses to migration and urban health in Hillbrow: the Johannesburg Migrant Health Forum

Research

Is laboratory screening prior to antiretroviral treatment useful in Johannesburg, South Africa? Baseline findings of a clinical trial