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 1/2017

Open Access 01-12-2017 | Research article

Prevalence of oncogenic human papillomavirus genotypes in patients diagnosed with anogenital malignancies in Botswana

Authors: Patricia S. Rantshabeng, Sikhulile Moyo, Natasha O. Moraka, Andrew Ndlovu, Iain J. MacLeod, Simani Gaseitsiwe, Ishmael Kasvosve

Published in: BMC Infectious Diseases | Issue 1/2017

Login to get access

Abstract

Background

Human papillomavirus (HPV) associated malignancies are the leading cause of cancer death in Botswana. We sought to determine causative HPV types in patients with anogenital malignancies in Botswana to inform vaccine strategy.

Methods

We used formalin-fixed and paraffin-embedded (FFPE) tissue blocks from patients diagnosed with anal, penile and vulvar squamous cell carcinomas between the years, 2014 and 2016. Presence of HPV 16, 18, or other high-risk (HR) types was detected using Abbott m2000 real-time PCR platform. Tissues with other high-risk types were subsequently analysed using a multiplex qPCR assay that includes 15 validated fluorophore probes.

Results

A total of 126 tissue specimens, comprising of 21 anal (9 males, 12 females), 31 penile and 74 vulvar were studied. Ninety-three (73.8%) patients had their HIV status documented in the records while the rest did not. Eighty-three (83) out of 93 were HIV positive, a prevalence of 89.4% (95% CI: 81–94). HPV was detected in 68/126 (54%) tissues, of which 69% (95% CI: 54–79) had HPV 16 only, 28% (95% CI: 19–40) had other hr.-HPV types and 2.9% (95% CI, 3.5–10.1) were co-infected with HPV 16 and other hr.-types. Other high-risk types detected included HPV 26, 31, 33, 35, 39, 45, 51, 52, 66 and 68. HPV 18 was not detected. Multiple-type HPV infection was detected in 44 of 47 (93.6%) HIV positive participants co-infected with HPV. In HIV-negative individuals, only HPV 16 was detected.

Conclusion

In our study, anogenital carcinomas were associated with HPV 16 and other hr.-HPV types besides HPV 16 and 18. HIV co-infected patients had multiple hr.-HPV types detected whereas in HIV-negative patients only HPV 16 was detected. Our study suggests that multivalent vaccines may be more suitable in this setting, especially for HIV-infected individuals.
Literature
1.
Bosch FX, Broker TR, Forman D, Moscicki A-B, Gillison ML, Doorbar J, Stern PL, Stanley M, Arbyn M, Poljak M, et al. Comprehensive Control of Human Papillomavirus Infections and Related Diseases. Vaccine. 2013;31(0 8):I1–31.CrossRefPubMedPubMedCentral
2.
De Vuyst H, Alemany L, Lacey C, Chibwesha CJ, Sahasrabuddhe V, Banura C, Denny L, Parham GP. The Burden of Human Papillomavirus Infections and Related Diseases in Sub-Saharan Africa. Vaccine. 2013;31(0 5):F32–46.CrossRefPubMedPubMedCentral
3.
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;30(Suppl 5):F12–23.CrossRefPubMed
4.
Dryden-Peterson S, Medhin H, Kebabonye-Pusoentsi M, Seage GR 3rd, Suneja G, Kayembe MK, Mmalane M, Rebbeck T, Rider JR, Essex M, et al. Cancer incidence following expansion of HIV treatment in Botswana. PLoS One. 2015;10(8):e0135602.CrossRefPubMedPubMedCentral
5.
Coleman N, Birley HD, Renton AM, Hanna NF, Ryait BK, Byrne M, Taylor-Robinson D, Stanley MA. Immunological events in regressing genital warts. Am J Clin Pathol. 1994;102(6):768–74.CrossRefPubMed
6.
Strickler HD, Burk RD, Fazzari M, Anastos K, Minkoff H, Massad LS, Hall C, Bacon M, Levine AM, Watts DH, 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
7.
8.
9.
Moscicki AB, Ellenberg JH, Farhat S, Xu J. Persistence of human papillomavirus infection in HIV-infected and -uninfected adolescent girls: risk factors and differences, by phylogenetic type. J Infect Dis. 2004;190(1):37–45.CrossRefPubMed
10.
Konopnicki D, Manigart Y, Gilles C, Barlow P, de Marchin J, Feoli F, Larsimont D, Delforge M, De Wit S, Clumeck N. High-risk human papillomavirus infection in HIV-positive African women living in Europe. J Int AIDS Soc. 2013;16(1):18023.CrossRefPubMedPubMedCentral
11.
12.
Averbach SH, Gravitt PE, Nowak RG, Celentano DD, Dunbar MS, Morrison CS, Grimes B, Padian NS. The association between cervical human papillomavirus infection and HIV acquisition among women in Zimbabwe. AIDS. 2010;24(7):1035–42.CrossRefPubMedPubMedCentral
13.
Smith JS, Moses S, Hudgens M, Parker CB, Agot K, Maclean I, Ndinya-Achola JO, Snijders PJF, Meijer C, Bailey RC. Increased risk of HIV acquisition among Kenyan men with human papillomavirus infection. J Infect Dis. 2010;201(11):1677–85.CrossRefPubMedPubMedCentral
14.
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
15.
16.
Phanuphak N, Teeratakulpisarn N, Pankam T, Kerr SJ, Barisri J, Deesua A, Rodbamrung P, Hongchookiat P, Chomchey N, Phanuphak P, et al. Anal human papillomavirus infection among Thai men who have sex with men with and without HIV infection: prevalence, incidence, and persistence. J Acquir Immune Defic Syndr. 2013;63(4):472–9.CrossRefPubMedPubMedCentral
17.
Simbiri KO, Jha HC, Kayembe MK, Kovarik C, Robertson ES. Oncogenic viruses associated with vulva cancer in HIV-1 patients in Botswana. Infect Agent Cancer. 2014;9:28.CrossRefPubMedPubMedCentral
18.
Castle PE, Stoler MH, Wright TC Jr, Sharma A, Wright TL, Behrens CM. Performance of carcinogenic human papillomavirus (HPV) testing and HPV16 or HPV18 genotyping for cervical cancer screening of women aged 25 years and older: a subanalysis of the ATHENA study. Lancet Oncol. 2011;12(9):880–90.CrossRefPubMed
19.
Bosch FX, Lorincz A, Munoz N, Meijer CJ, Shah KV. The causal relation between human papillomavirus and cervical cancer. J Clin Pathol. 2002;55(4):244–65.CrossRefPubMedPubMedCentral
20.
Bernard HU. The clinical importance of the nomenclature, evolution and taxonomy of human papillomaviruses. J Clin Virol. 2005;32(Suppl 1):S1–6.CrossRefPubMed
21.
Ault KA, Giuliano AR, Edwards RP, Tamms G, Kim LL, Smith JF, Jansen KU, Allende M, Taddeo FJ, Skulsky D, et al. A phase I study to evaluate a human papillomavirus (HPV) type 18 L1 VLP vaccine. Vaccine. 2004;22(23–24):3004–7.CrossRefPubMed
22.
Parkin DM. The global health burden of infection-associated cancers in the year 2002. Int J Cancer. 2006;118(12):3030–44.CrossRefPubMed
23.
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
24.
Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, et al. A review of human carcinogens--part B: biological agents. Lancet Oncol. 2009;10(4):321–2.CrossRefPubMed
25.
Malagon T, Drolet M, Boily MC, Franco EL, Jit M, Brisson J, Brisson M. Cross-protective efficacy of two human papillomavirus vaccines: a systematic review and meta-analysis. Lancet Infect Dis. 2012;12(10):781–9.CrossRefPubMed
26.
Ermel A, Ramogola-Masire D, Zetola N, Tong Y, Qadadri B, Azar MM, Brown DR. Invasive cervical cancers from women living in the United States or Botswana: differences in human papillomavirus type distribution. Infect Agent Cancer. 2014;9:22.CrossRefPubMedPubMedCentral
27.
Ermel A, Qadadri B, Tong Y, Orang'o O, Macharia B, Ramogola-Masire D, Zetola NM, Brown DR. Invasive cervical cancers in the United States, Botswana and Kenya: HPV type distribution and health policy implications. Infect Agent Cancer. 2016;11:56.CrossRefPubMedPubMedCentral
28.
DiAngi YT, Panozzo CA, Ramogola-Masire D, Steenhoff AP, Brewer NT. A cross-sectional study of HPV vaccine acceptability in Gaborone, Botswana. PLoS One. 2011;6(10):e25481.CrossRefPubMedPubMedCentral
29.
Ramogola-Masire D, McGrath CM, Barnhart KT, Friedman HM, Zetola NM. Subtype distribution of human papillomavirus in HIV-infected women with cervical intraepithelial neoplasia stages 2 and 3 in Botswana. Int J Gynecol Pathol. 2011;30(6):591–6.CrossRefPubMedPubMedCentral
30.
MacLeod IJ, O'Donnell B, Moyo S, Lockman S, Shapiro RL, Kayembe M, van Widenfelt E, Makhema J, Essex M, Wester C. Prevalence of human papillomavirus genotypes and associated cervical squamous intraepithelial lesions in HIV-infected women in Botswana. J Med Virol. 2011;83(10):1689–95.CrossRefPubMedPubMedCentral
31.
Poljak M, Ostrbenk A. The Abbott RealTime high risk HPV test is a clinically validated human papillomavirus assay for triage in the referral population and use in primary cervical cancer screening in women 30 years and older: a review of validation studies. Acta dermatovenerologica Alpina, Pannonica, et Adriatica. 2013;22(2):43–7.PubMed
32.
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
33.
Delany-Moretlwe S, Bello B, Kinross P, Oliff M, Chersich M, Kleinschmidt I, Rees H. HIV prevalence and risk in long-distance truck drivers in South Africa: a national cross-sectional survey. Int J STD AIDS. 2014;25(6):428–38.CrossRefPubMed
34.
Houlihan CF, Larke NL, Watson-Jones D, KK S-MC, Shiboski S, Gravitt PE, et al. HPV infection and increased risk of HIV acquisition: a systematic review and meta-analysis. AIDS. 2012;26(17):2211–22.CrossRefPubMed
35.
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
36.
Grover S, Raesima M, Bvochora-Nsingo M, Chiyapo SP, Balang D, Tapela N, Balogun O, Kayembe MK, Russell AH, Monare B, et al. Cervical cancer in Botswana: current state and future steps for screening and treatment programs. Front Oncol. 2015;5:239.PubMedPubMedCentral
37.
Levi JE, Kleter B, Quint WG, Fink MC, Canto CL, Matsubara R. 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
38.
Menon S, van den Broeck D, Rossi R, Ogbe E, Mabeya H, Multiple HPV. Infections in female sex workers in western Kenya: implications for prophylactic vaccines within this sub population. Infect Agent Cancer. 2017;12(1):2.CrossRefPubMedPubMedCentral
39.
Palefsky JM, Minkoff H, Kalish LA, Levine A, Sacks HS, Garcia P, Young M, Melnick S, Miotti P, Burk R. Cervicovaginal human papillomavirus infection in human immunodeficiency virus-1 (HIV)-positive and high-risk HIV-negative women. J Natl Cancer Inst. 1999;91(3):226–36.CrossRefPubMed
40.
Ahdieh L, Klein RS, Burk R, Cu-Uvin S, Schuman P, Duerr A, Safaeian M, Astemborski J, Daniel R, Shah K. Prevalence, incidence, and type-specific persistence of human papillomavirus in human immunodeficiency virus (HIV)-positive and HIV-negative women. J Infect Dis. 2001;184(6):682–90.CrossRefPubMed
41.
Ng’andwe C, Lowe JJ, Richards PJ, Hause L, Wood C, Angeletti PC. The distribution of sexually-transmitted human papillomaviruses in HIV positive and negative patients in Zambia, Africa. BMC Infect Dis. 2007;7:77.CrossRefPubMedPubMedCentral
42.
Russomano F, Paz BR, Camargo MJ, Grinstejn BG, Friedman RK, Tristao MA, Oliveira CA. Recurrence of cervical intraepithelial neoplasia in human immunodeficiency virus-infected women treated by means of electrosurgical excision of the transformation zone (LLETZ) in Rio de Janeiro, Brazil. Sao Paulo Med J. 2013;131(6):405–10.PubMed
43.
Mu Mu S, Hlaing Myat T, Khin Saw A, Aye Aye M, Mya T, Khin Shwe M, Khin Khin O, Khin Sandar A, Okada S, Kyaw Zin T. Determination of oncogenic human papillomavirus (HPV) genotypes in Anogenital cancers in Myanmar. Acta Med Okayama. 2016;70(2):103–10.
44.
Rubin MA, Kleter B, Zhou M, Ayala G, Cubilla AL, Quint WG, Pirog EC. Detection and typing of human papillomavirus DNA in penile carcinoma: evidence for multiple independent pathways of penile carcinogenesis. Am J Pathol. 2001;159(4):1211–8.CrossRefPubMedPubMedCentral
45.
Heideman DA, Waterboer T, Pawlita M, Delis-van Diemen P, Nindl I, Leijte JA, Bonfrer JM, Horenblas S, Meijer CJ, Snijders PJ. Human papillomavirus-16 is the predominant type etiologically involved in penile squamous cell carcinoma. J Clin Oncol. 2007;25(29):4550–6.CrossRefPubMed
46.
McCance DJ, Kalache A, Ashdown K, Andrade L, Menezes F, Smith P, Doll R. Human papillomavirus types 16 and 18 in carcinomas of the penis from Brazil. Int J Cancer. 1986;37(1):55–9.CrossRefPubMed
47.
Newton R, Bousarghin L, Ziegler J, Casabonne D, Beral V, Mbidde E, Carpenter L, Parkin DM, Wabinga H, Mbulaiteye S, et al. Human papillomaviruses and cancer in Uganda. Eur J Cancer Prev. 2004;13(2):113–8.CrossRefPubMed
48.
Lebelo RL, Boulet G, Nkosi CM, Bida MN, Bogers JP, Mphahlele MJ. Diversity of HPV types in cancerous and pre-cancerous penile lesions of south African men: implications for future HPV vaccination strategies. J Med Virol. 2014;86(2):257–65.CrossRefPubMed
49.
Daling JR, Madeleine MM, Johnson LG, Schwartz SM, Shera KA, Wurscher MA, Carter JJ, Porter PL, Galloway DA, McDougall JK, et al. Penile cancer: importance of circumcision, human papillomavirus and smoking in in situ and invasive disease. Int J Cancer. 2005;116(4):606–16.CrossRefPubMed
50.
Daling JR, Sherman KJ. Relationship between human papillomavirus infection and tumours of anogenital sites other than the cervix. IARC Sci Publ. 1992;119:223–41.
51.
Van Doornum GJ, Prins M, Juffermans LH, Hooykaas C, van den Hoek JA, Coutinho RA, Quint WG. Regional distribution and incidence of human papillomavirus infections among heterosexual men and women with multiple sexual partners: a prospective study. Genitourin Med. 1994;70(4):240–6.PubMedPubMedCentral
52.
Palefsky JM, Gillison ML, Strickler HD. Chapter 16: HPV vaccines in immunocompromised women and men. Vaccine. 2006;24(Suppl 3):S3/140–6.
53.
Frisch M. On the etiology of anal squamous carcinoma. Dan Med Bull. 2002;49(3):194–209.PubMed
54.
Bruni L, Diaz M, Castellsague X, Ferrer E, Bosch FX, de Sanjose S. Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J Infect Dis. 2010;202(12):1789–99.CrossRefPubMed
55.
Didelot-Rousseau MN, Nagot N, Costes-Martineau V, Valles X, Ouedraogo A, Konate I, Weiss HA, Perre P, Mayaud P, Segondy M. Human papillomavirus genotype distribution and cervical squamous intraepithelial lesions among high-risk women with and without HIV-1 infection in Burkina Faso. Br J Cancer. 2006;95(3):355–62.CrossRefPubMedPubMedCentral
56.
Akarolo-Anthony SN, Al-Mujtaba M, Famooto AO, Dareng EO, Olaniyan OB, Offiong R, Wheeler CM, Adebamowo CA. HIV associated high-risk HPV infection among Nigerian women. BMC Infect Dis. 2013;13:521.CrossRefPubMedPubMedCentral
57.
Riethmuller D, Jacquard AC, Lacau St Guily J, Aubin F, Carcopino X, Pradat P, Dahlab A, Pretet JL. Potential impact of a nonavalent HPV vaccine on the occurrence of HPV-related diseases in France. BMC Public Health. 2015;15:453.CrossRefPubMedPubMedCentral
58.
Serrano B, de Sanjose S, Tous S, Quiros B, Munoz N, Bosch X, Alemany L. Human papillomavirus genotype attribution for HPVs 6, 11, 16, 18, 31, 33, 45, 52 and 58 in female anogenital lesions. Eur J Cancer. 2015;51(13):1732–41.CrossRefPubMed
59.
Grover S, Raesima M, Bvochora-Nsingo M, Chiyapo SP, Balang D, Tapela N, Balogun O, Kayembe MKA, Russell AH, Monare B, et al. Cervical cancer in Botswana: current state and future steps for screening and treatment programs. Front Oncol. 2015;5:239.PubMedPubMedCentral
60.
Raesima MM, Forhan SE, Voetsch AC, Hewitt S, Hariri S, Wang SA, Pelletier AR, Letebele M, Pheto T, Ramogola-Masire D, et al. Human papillomavirus vaccination coverage among school girls in a demonstration project - Botswana, 2013. MMWR Morb Mortal Wkly Rep. 2015;64(40):1147–9.CrossRefPubMed
Metadata
Title
Prevalence of oncogenic human papillomavirus genotypes in patients diagnosed with anogenital malignancies in Botswana
Authors
Patricia S. Rantshabeng
Sikhulile Moyo
Natasha O. Moraka
Andrew Ndlovu
Iain J. MacLeod
Simani Gaseitsiwe
Ishmael Kasvosve
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2017
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-017-2832-8

Other articles of this Issue 1/2017

BMC Infectious Diseases 1/2017 Go to the issue

Research article

Durability of switch regimens based on rilpivirine or on integrase inhibitors, both in association with tenofovir and emtricitabine, in HIV-infected, virologically suppressed patients

Research article

Identifying and characterizing hepatitis C virus hotspots in Massachusetts: a spatial epidemiological approach

Research article

Seroprevalence and risk factors of brucellosis in abattoir workers at Debre Zeit and Modjo export abattoir, Central Ethiopia

Research article

Genotypes of hepatitis a virus in Turkey: first report and clinical profile of children infected with sub-genotypes IA and IIIA

Research article

Age-standardized mortality rates related to viral hepatitis in Brazil

Research article

Valine/isoleucine variants drive selective pressure in the VP1 sequence of EV-A71 enteroviruses
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