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 Infectious Diseases
Published in: BMC Infectious Diseases 1/2015

Open Access 01-12-2015 | Research article

Human papillomavirus prevalence in South African women and men according to age and human immunodeficiency virus status

Authors: Zizipho Z A Mbulawa, David Coetzee, Anna-Lise Williamson

Published in: BMC Infectious Diseases | Issue 1/2015

Login to get access

Abstract

Background

Both cervical cancer and human immunodeficiency virus (HIV) are major public health problems in Sub-Saharan Africa. The objectives of the study were to investigate human papillomavirus (HPV) prevalence according to age, HIV status and gender.

Methods

Participants were 208 HIV-negative women, 278 HIV-positive women, 325 HIV-negative men and 161 HIV-positive men between the ages of 18–66 years. HPV types were determined in cervical and penile cells by Roche Linear Array HPV genotyping assay.

Results

HPV prevalence was 36.7 % (76/207; 95 % confidence intervals (CI): 30.4–43.4 %) in HIV-negative women, with the highest prevalence of 61.0 % (25/41; 95 % CI: 45.7–74.4 %) in women aged 18–25 years. HPV prevalence was 74.0 % (205/277; 95 % CI: 68.5–78.8 %) in HIV-positive women, with the highest prevalence of 86.4 % (38/44; 95 % CI: 72.9–94.0 %) in women aged 18–25 years. HPV prevalence was found to decrease with increasing age in HIV-negative women (P = 0.0007), but not in HIV-positive women (P = 0.898). HPV prevalence was 50.8 % (159/313; 95 % CI: 45.3–56.3 %) in HIV-negative men, with the highest prevalence of 77.0 % (27/35; 95 % CI: 60.7–88.2 %) in men aged 18–25 years. HPV prevalence was 76.6 % (121/158; 95 % CI: 69.2–82.9 %) in HIV-positive men, with the highest prevalence of 87.5 % (7/8; 95 % CI: 50.8–99.9 %) in men 18–25 years of age. HPV prevalence was found to decrease with increasing age in HIV-negative men (P = 0.004), but not in HIV-positive men (P = 0.385). HIV-positive women had a significantly higher prevalence of one or more HPV type(s) in the bivalent (HPV-16/18: 20 % 55/277, 9 % 12/207; P <0.001), quadrivalent (HPV-6/11/16/18: 26 % 71/277, 12 % 24/207; P = 0.001) and nonavalent vaccine (HPV-6/11/16/18/31/33/52/56/58: 65 % 181/277, 24 % 50/207; P <0.001) compared to HIV-negative women. Similar observation were observed in men for bivalent (20 % 32/158, 10 % 30/313; P = 0.001), quadrivalent (35 % 56/158, 13 % 41/313; P <0.001) and nonavalent vaccine (75 % 119/158, 28 % 87/313; P <0.001).

Conclusions

This study demonstrated high HPV prevalence among HIV-positive women and men in all age groups. The high prevalence of HPV types found in bivalent, quadrivalent and nonavalent vaccines in South African HIV-positive and HIV-negative women and men demonstrate that this population will greatly benefit from current HPV vaccines.
Literature
1.
UNAIDS’s push to end epidemic. Science. 2014;346(6213):1036.
2.
Who U, Unicef. Global report: UNAIDS report on the global AIDS epidemic 2013. Geneva: UNAIDS; 2013.
3.
Naicker N, Kharsany AB, Werner L, van Loggerenberg F, Mlisana K, Garrett N, et al. Risk factors for HIV acquisition in high risk women in a generalised epidemic setting. AIDS Behav. 2015;19(7):1305–16.CrossRefPubMedPubMedCentral
4.
MacPhail C, Williams BG, Campbell C. Relative risk of HIV infection among young men and women in a South African township. Int J STD AIDS. 2002;13(5):331–42.CrossRefPubMed
5.
Kelly RJ, Gray RH, Sewankambo NK, Serwadda D, Wabwire-Mangen F, Lutalo T, et al. Age differences in sexual partners and risk of HIV-1 infection in rural Uganda. J Acquir Immune Defic Syndr. 2003;32(4):446–51.CrossRefPubMed
6.
Pettifor AE, Rees HV, Kleinschmidt I, Steffenson AE, MacPhail C, Hlongwa-Madikizela L, et al. Young people’s sexual health in South Africa: HIV prevalence and sexual behaviors from a nationally representative household survey. Aids. 2005;19(14):1525–34.CrossRefPubMed
7.
Jewkes R, Dunkle K, Nduna M, Levin J, Jama N, Khuzwayo N, et al. Factors associated with HIV sero-status in young rural South African women: connections between intimate partner violence and HIV. Int J Epidemiol. 2006;35(6):1461–8.CrossRefPubMed
8.
9.
de Sanjose S, Diaz M, Castellsague X, Clifford G, Bruni L, Munoz N, et al. Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect Dis. 2007;7(7):453–9.CrossRefPubMed
10.
Vinodhini K, Shanmughapriya S, Das BC, Natarajaseenivasan K. Prevalence and risk factors of HPV infection among women from various provinces of the world. Arch Gynecol Obstet. 2012;285(3):771–7.CrossRefPubMed
11.
Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010;127(12):2893–917.CrossRefPubMed
12.
Lissouba P, Van de Perre P, Auvert B. Association of genital human papillomavirus infection with HIV acquisition: a systematic review and meta-analysis. Sex Transm Infect. 2013;89(5):350–6.CrossRefPubMedPubMedCentral
13.
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(1):15–27.CrossRefPubMed
14.
Smits PH, Bakker R, Jong E, Mulder JW, Meenhorst PL, Kleter B, et al. High prevalence of human papillomavirus infections in urine samples from human immunodeficiency virus-infected men. J Clin Microbiol. 2005;43(12):5936–9.CrossRefPubMedPubMedCentral
15.
Heard I, Tassie JM, Schmitz V, Mandelbrot L, Kazatchkine MD, Orth G. Increased risk of cervical disease among human immunodeficiency virus-infected women with severe immunosuppression and high human papillomavirus load(1). Obstet Gynecol. 2000;96(3):403–9.PubMed
16.
Riva E, Serraino D, Pierangeli A, Bambacioni F, Zaniratti S, Minosse C, et al. Markers of human papillomavirus infection and their correlation with cervical dysplasia in human immunodeficiency virus-positive women. Clin Microbiol Infect. 2007;13(1):94–7.CrossRefPubMed
17.
Levi JE, Fernandes S, Tateno AF, Motta E, Lima LP, Eluf-Neto J, et al. Presence of multiple human papillomavirus types in cervical samples from HIV-infected women. Gynecol Oncol. 2004;92(1):225–31.CrossRefPubMed
18.
Levi JE, Kleter B, Quint WG, Fink MC, Canto CL, Matsubara R, et al. High prevalence of human papillomavirus (HPV) infections and high frequency of multiple HPV genotypes in human immunodeficiency virus-infected women in Brazil. J Clin Microbiol. 2002;40(9):3341–5.CrossRefPubMedPubMedCentral
19.
Strickler HD, Burk RD, Fazzari M, Anastos K, Minkoff H, Massad LS, et al. Natural history and possible reactivation of human papillomavirus in human immunodeficiency virus-positive women. J Natl Cancer Inst. 2005;97(8):577–86.CrossRefPubMed
20.
Lomalisa P, Smith T, Guidozzi F. Human immunodeficiency virus infection and invasive cervical cancer in South Africa. Gynecol Oncol. 2000;77(3):460–3.CrossRefPubMed
21.
Frisch M, Biggar RJ, Goedert JJ. Human papillomavirus-associated cancers in patients with human immunodeficiency virus infection and acquired immunodeficiency syndrome. J Natl Cancer Inst. 2000;92(18):1500–10.CrossRefPubMed
22.
Chin-Hong PV, Husnik M, Cranston RD, Colfax G, Buchbinder S, Da Costa M, et al. Anal human papillomavirus infection is associated with HIV acquisition in men who have sex with men. Aids. 2009;23(9):1135–42.CrossRefPubMedPubMedCentral
23.
Auvert B, Lissouba P, Cutler E, Zarca K, Puren A, Taljaard D. Association of oncogenic and nononcogenic human papillomavirus with HIV incidence. J Acquir Immune Defic Syndr. 2010;53(1):111–6.CrossRefPubMedPubMedCentral
24.
Auvert B, Sobngwi-Tambekou J, Cutler E, Nieuwoudt M, Lissouba P, Puren A, et al. 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
25.
Smith JS, Moses S, Hudgens MG, Parker CB, Agot K, Maclean I, et al. Increased risk of HIV acquisition among Kenyan men with human papillomavirus infection. J Infect Dis. 2010;201(11):1677–85.CrossRefPubMedPubMedCentral
26.
Smith-McCune KK, Shiboski S, Chirenje MZ, Magure T, Tuveson J, Ma Y, et al. Type-specific cervico-vaginal human papillomavirus infection increases risk of HIV acquisition independent of other sexually transmitted infections. PLoS One. 2010;5(4):e10094.CrossRefPubMedPubMedCentral
27.
Averbach SH, Gravitt PE, Nowak RG, Celentano DD, Dunbar MS, Morrison CS, et al. The association between cervical human papillomavirus infection and HIV acquisition among women in Zimbabwe. Aids. 2010;24(7):1035–42.CrossRefPubMedPubMedCentral
28.
Veldhuijzen NJ, Vyankandondera J, van de Wijgert JH. HIV acquisition is associated with prior high-risk human papillomavirus infection among high-risk women in Rwanda. Aids. 2010;24(14):2289–92.CrossRefPubMed
29.
Houlihan CF, Larke NL, Watson-Jones D, Smith-McCune KK, Shiboski S, Gravitt PE, et al. Human papillomavirus infection and increased risk of HIV acquisition. A systematic review and meta-analysis. Aids. 2012;26(17):2211–22.CrossRefPubMed
30.
Rositch AF, Gravitt PE, Smith JS. Growing evidence that HPV infection is associated with an increase in HIV acquisition: exploring the issue of HPV vaccination. Sex Transm Infect. 2013;89(5):357.CrossRefPubMed
31.
Joura EA, Giuliano AR, Iversen OE, Bouchard C, Mao C, Mehlsen J, et al. A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women. N Engl J Med. 2015;372(8):711–23.CrossRefPubMed
32.
Joura EA, Leodolter S, Hernandez-Avila M, Wheeler CM, Perez G, Koutsky LA, et al. Efficacy of a quadrivalent prophylactic human papillomavirus (types 6, 11, 16, and 18) L1 virus-like-particle vaccine against high-grade vulval and vaginal lesions: a combined analysis of three randomised clinical trials. Lancet. 2007;369(9574):1693–702.CrossRefPubMed
33.
Garland SM, Hernandez-Avila M, Wheeler CM, Perez G, Harper DM, Leodolter S, et al. Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N Engl J Med. 2007;356(19):1928–43.CrossRefPubMed
34.
Paavonen J, Naud P, Salmeron J, Wheeler CM, Chow SN, Apter D, et al. Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women. Lancet. 2009;374(9686):301–14.CrossRefPubMed
35.
Palefsky JM, Giuliano AR, Goldstone S, Moreira Jr ED, Aranda C, Jessen H, et al. HPV vaccine against anal HPV infection and anal intraepithelial neoplasia. N Engl J Med. 2011;365(17):1576–85.CrossRefPubMed
36.
Giuliano AR, Palefsky JM, Goldstone S, Moreira Jr ED, Penny ME, Aranda C, et al. Efficacy of quadrivalent HPV vaccine against HPV Infection and disease in males. N Engl J Med. 2011;364(5):401–11.CrossRefPubMedPubMedCentral
37.
Tiggelaar SM, Lin MJ, Viscidi RP, Ji J, Smith JS. Age-specific human papillomavirus antibody and deoxyribonucleic acid prevalence: a global review. J Adolesc Health. 2012;50(2):110–31.CrossRefPubMedPubMedCentral
38.
Smith JS, Melendy A, Rana RK, Pimenta JM. Age-specific prevalence of infection with human papillomavirus in females: a global review. J Adolesc Health. 2008;43(4 Suppl):S5–25. S25.e21-41.PubMed
39.
Olesen TB, Iftner T, Mwaiselage J, Kahesa C, Rasch V, Ngoma T, et al. 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
40.
Olesen TB, Munk C, Christensen J, Andersen KK, Kjaer SK. Human papillomavirus prevalence among men in sub-Saharan Africa: a systematic review and meta-analysis. Sex Transm Infect. 2014;90(6):455–62.CrossRefPubMed
41.
Giuliano AR, Lazcano-Ponce E, Villa LL, Flores R, Salmeron J, Lee JH, et al. The human papillomavirus infection in men study: human papillomavirus prevalence and type distribution among men residing in Brazil, Mexico, and the United States. Cancer Epidemiol Biomark Prev. 2008;17(8):2036–43.CrossRef
42.
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
43.
Mbulawa ZZ, Coetzee D, Marais DJ, Kamupira M, Zwane E, Allan B, et al. Genital human papillomavirus prevalence and human papillomavirus concordance in heterosexual couples are positively associated with human immunodeficiency virus coinfection. J Infect Dis. 2009;199(10):1514–24.CrossRefPubMed
44.
Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, et al. A review of human carcinogens—Part B: biological agents. Lancet Oncol. 2009;10(4):321–2.CrossRefPubMed
45.
Mbulawa ZZ, Johnson LF, Marais DJ, Gustavsson I, Moodley JR, Coetzee D, et al. Increased alpha-9 human papillomavirus species viral load in human immunodeficiency virus positive women. BMC Infect Dis. 2014;14:51.CrossRefPubMedPubMedCentral
46.
Mbulawa ZZ, Marais DJ, Johnson LF, Boulle A, Coetzee D, Williamson AL. Influence of human immunodeficiency virus and CD4 count on the prevalence of human papillomavirus in heterosexual couples. J Gen Virol. 2010;91(Pt 12):3023–31.CrossRefPubMed
47.
Mbulawa ZZ, Johnson LF, Marais DJ, Coetzee D, Williamson AL. The impact of human immunodeficiency virus on human papillomavirus transmission in heterosexually active couples. J Infect. 2013;67(1):51–8.CrossRefPubMed
48.
Simbayi L, Shisana O, Rehle T, Onoya D, Jooste S, Zungu N, et al. South African national HIV prevalence, incidence and behaviour survey, 2012. Pretoria: Human Sciences Research Council; 2014.
49.
Myer L, Phillips T, Manuelli V, McIntyre J, Bekker LG, Abrams EJ. Evolution of antiretroviral therapy services for HIV-infected pregnant women in Cape Town, South Africa. J Acquir Immune Defic Syndr. 2015. [Epub ahead of print].
50.
Forman D, de Martel C, Lacey CJ, Soerjomataram I, Lortet-Tieulent J, Bruni L, et al. Global burden of human papillomavirus and related diseases. Vaccine. 2012;30 Suppl 5:F12–23.CrossRefPubMed
51.
Cuschieri KS, Cubie HA, Whitley MW, Seagar AL, Arends MJ, Moore C, et al. Multiple high risk HPV infections are common in cervical neoplasia and young women in a cervical screening population. J Clin Pathol. 2004;57(1):68–72.CrossRefPubMedPubMedCentral
52.
Kjaer SK, Svare EI, Worm AM, Walboomers JM, Meijer CJ, van den Brule AJ. Human papillomavirus infection in Danish female sex workers. Decreasing prevalence with age despite continuously high sexual activity. Sex Transm Dis. 2000;27(8):438–45.CrossRefPubMed
53.
Giuliano AR, Botha MH, Zeier M, Abrahamsen ME, Glashoff RH, van der Laan LE, et al. High HIV, HPV, and STI prevalence among Young Western Cape, South African Women: EVRI HIV prevention preparedness trial. J Acquir Immune Defic Syndr. 2015;68(2):227–35.CrossRefPubMedPubMedCentral
54.
McDonald AC, Tergas AI, Kuhn L, Denny L, Wright Jr TC. Distribution of Human Papillomavirus genotypes among HIV-positive and HIV-negative Women in Cape Town, South Africa. Front Oncol. 2014;4:48.CrossRefPubMedPubMedCentral
55.
Richter K, Becker P, Horton A, Dreyer G. Age-specific prevalence of cervical human papillomavirus infection and cytological abnormalities in women in Gauteng Province, South Africa. S Afr Med J. 2013;103(5):313–7.CrossRefPubMed
56.
Giuliano AR, Harris R, Sedjo RL, Baldwin S, Roe D, Papenfuss MR, et al. Incidence, prevalence, and clearance of type-specific human papillomavirus infections: The Young Women’s Health Study. J Infect Dis. 2002;186(4):462–9.CrossRefPubMed
57.
Andersson S, Safari H, Mints M, Lewensohn-Fuchs I, Gyllensten U, Johansson B. Type distribution, viral load and integration status of high-risk human papillomaviruses in pre-stages of cervical cancer (CIN). Br J Cancer. 2005;92(12):2195–200.CrossRefPubMedPubMedCentral
58.
Munoz N, Castellsague X, de Gonzalez AB, Gissmann L. Chapter 1: HPV in the etiology of human cancer. Vaccine. 2006;24 Suppl 3:S3/1–10.
59.
Trottier H, Mahmud S, Prado JC, Sobrinho JS, Costa MC, Rohan TE, et al. Type-specific duration of human papillomavirus infection: implications for human papillomavirus screening and vaccination. J Infect Dis. 2008;197(10):1436–47.CrossRefPubMed
60.
Munagala R, Dona MG, Rai SN, Jenson AB, Bala N, Ghim SJ, et al. Significance of multiple HPV infection in cervical cancer patients and its impact on treatment response. Int J Oncol. 2009;34(1):263–71.PubMed
61.
Bello BD, Spinillo A, Alberizzi P, Cesari S, Gardella B, D’Ambrosio G, et al. Cervical infections by multiple human papillomavirus (HPV) genotypes: prevalence and impact on the risk of precancerous epithelial lesions. J Med Virol. 2009;81(4):703–12.CrossRefPubMed
62.
Jones HE, Allan BR, van de Wijgert JH, Altini L, Taylor SM, de Kock A, et al. Agreement between self- and clinician-collected specimen results for detection and typing of high-risk human papillomavirus in specimens from women in Gugulethu, South Africa. J Clin Microbiol. 2007;45(6):1679–83.CrossRefPubMedPubMedCentral
Metadata
Title
Human papillomavirus prevalence in South African women and men according to age and human immunodeficiency virus status
Authors
Zizipho Z A Mbulawa
David Coetzee
Anna-Lise Williamson
Publication date
01-12-2015
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2015
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-015-1181-8

Other articles of this Issue 1/2015

BMC Infectious Diseases 1/2015 Go to the issue

Research article

Treatment outcomes in multidrug resistant tuberculosis-human immunodeficiency virus Co-infected patients on anti-retroviral therapy at Sizwe Tropical Disease Hospital Johannesburg, South Africa

Research article

Necrotizing fasciitis in patients with diabetes mellitus: clinical characteristics and risk factors for mortality

Research article

Urinary Neutrophil Gelatinase-Associated Lipocalin (NGAL) and proteinuria predict severity of acute kidney injury in Puumala virus infection

Case report

Pleural effusion as the initial clinical presentation in disseminated cryptococcosis and fungaemia: an unusual manifestation and a literature review

Research article

Clonal dissemination of linezolid-resistant Staphylococcus capitis with G2603T mutation in domain V of the 23S rRNA and the cfr gene at a tertiary care hospital in China

Research article

CD14+ macrophages that accumulate in the colon of African AIDS patients express pro-inflammatory cytokines and are responsive to lipopolysaccharide
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

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

Pediatric Cardiology Video

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

Cardiopulmonary Comorbidity Video

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

Valvular Heart Disease Video

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

Heart Failure Video

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

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

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

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits