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Published in: BMC Infectious Diseases 1/2019

Open Access 01-12-2019 | Human Papillomavirus | Research article

Prevalence and incidence of genital warts and cervical Human Papillomavirus infections in Nigerian women

Authors: Eileen O. Dareng, Sally N. Adebamowo, Ayotunde Famooto, Oluwatoyosi Olawande, Michael K. Odutola, Yinka Olaniyan, Richard A. Offiong, Paul P. Pharoah, Clement A. Adebamowo

Published in: BMC Infectious Diseases | Issue 1/2019

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Abstract

Background

Genital warts are important causes of morbidity and their prevalence and incidence can be used to evaluate the impact of HPV vaccination in a population.

Methods

We enrolled 1020 women in a prospective cohort study in Nigeria and followed them for a mean (SD) of 9 (4) months. Nurses conducted pelvic examinations and collected ectocervical samples for HPV testing. We used exact logistic regression models to identify risk factors for genital warts.

Results

The mean age of study participants was 38 years, 56% (535/962) were HIV-negative and 44% (427/962) were HIV-positive. Prevalence of genital warts at enrolment was 1% (4/535) among HIV-negative women, and 5% (23/427) among HIV-positive women. Of 614 women (307 HIV negative and 307 HIV positive women) for whom we could compute genital wart incidence, it was 515 (95% CI:13–2872) per 100,000 person-years in HIV-negative and 1370 (95% CI:283–4033) per 100,000 person-years in HIV-positive women. HIV was associated with higher risk of prevalent genital warts (OR:7.14, 95% CI:2.41–28.7, p < 0.001) while higher number of sex partners in the past year was associated with increased risk of incident genital warts (OR:2.86, 95% CI:1.04–6.47. p = 0.04). HPV11 was the only HPV associated with prevalent genital warts in this population (OR:8.21, 95% CI:2.47–27.3, p = 0.001).

Conclusion

Genital warts are common in Nigeria and our results provide important parameters for monitoring the impact of future HPV vaccination programs in the country. HIV infection and number of sexual partners in past year were important risk factors for prevalent and incident genital warts respectively.
Literature
1.
go back to reference Fenton KA, Lowndes CM. Recent trends in the epidemiology of sexually transmitted infections in the European Union. Sex Transm Infect. 2004;80(4):255–63.CrossRef Fenton KA, Lowndes CM. Recent trends in the epidemiology of sexually transmitted infections in the European Union. Sex Transm Infect. 2004;80(4):255–63.CrossRef
2.
go back to reference Sugase M, Moriyama S, Matsukura T. Human papillomavirus in exophytic condylomatous lesions on different female genital regions. J Med Virol. 1991;34(1):1–6.CrossRef Sugase M, Moriyama S, Matsukura T. Human papillomavirus in exophytic condylomatous lesions on different female genital regions. J Med Virol. 1991;34(1):1–6.CrossRef
3.
go back to reference Doorbar J, Egawa N, Griffin H, Kranjec C, Murakami I. Human papillomavirus molecular biology and disease association. Rev Med Virol. 2015;25(Suppl 1):2–23.CrossRef Doorbar J, Egawa N, Griffin H, Kranjec C, Murakami I. Human papillomavirus molecular biology and disease association. Rev Med Virol. 2015;25(Suppl 1):2–23.CrossRef
4.
go back to reference Greer CE, Wheeler CM, Ladner MB, Beutner K, Coyne MY, Liang H, Langenberg A, Yen TS, Ralston R. Human papillomavirus (HPV) type distribution and serological response to HPV type 6 virus-like particles in patients with genital warts. J Clin Microbiol. 1995;33(8):2058–63.PubMedPubMedCentral Greer CE, Wheeler CM, Ladner MB, Beutner K, Coyne MY, Liang H, Langenberg A, Yen TS, Ralston R. Human papillomavirus (HPV) type distribution and serological response to HPV type 6 virus-like particles in patients with genital warts. J Clin Microbiol. 1995;33(8):2058–63.PubMedPubMedCentral
5.
go back to reference Patel H, Wagner M, Singhal P, Kothari S. Systematic review of the incidence and prevalence of genital warts. BMC Infect Dis. 2013;13:39.CrossRef Patel H, Wagner M, Singhal P, Kothari S. Systematic review of the incidence and prevalence of genital warts. BMC Infect Dis. 2013;13:39.CrossRef
6.
go back to reference Fonck K, Kidula N, Kirui P, Ndinya-Achola J, Bwayo J, Claeys P, Temmerman M. Pattern of sexually transmitted diseases and risk factors among women attending an STD referral clinic in Nairobi. Kenya Sex Transm Dis. 2000;27(7):417–23. Fonck K, Kidula N, Kirui P, Ndinya-Achola J, Bwayo J, Claeys P, Temmerman M. Pattern of sexually transmitted diseases and risk factors among women attending an STD referral clinic in Nairobi. Kenya Sex Transm Dis. 2000;27(7):417–23.
7.
go back to reference Smith MA, Liu B, McIntyre P, Menzies R, Dey A, Canfell K. Fall in genital warts diagnoses in the general and indigenous Australian population following implementation of a national human papillomavirus vaccination program: analysis of routinely collected national hospital data. J Infect Dis. 2015;211(1):91–9.CrossRef Smith MA, Liu B, McIntyre P, Menzies R, Dey A, Canfell K. Fall in genital warts diagnoses in the general and indigenous Australian population following implementation of a national human papillomavirus vaccination program: analysis of routinely collected national hospital data. J Infect Dis. 2015;211(1):91–9.CrossRef
8.
go back to reference Howell-Jones R, Soldan K, Wetten S, Mesher D, Williams T, Gill ON, Hughes G. Declining genital warts in young women in England associated with HPV 16/18 vaccination: an ecological study. J Infect Dis. 2013;208(9):1397–403.CrossRef Howell-Jones R, Soldan K, Wetten S, Mesher D, Williams T, Gill ON, Hughes G. Declining genital warts in young women in England associated with HPV 16/18 vaccination: an ecological study. J Infect Dis. 2013;208(9):1397–403.CrossRef
9.
go back to reference 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.CrossRef 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.CrossRef
10.
go back to reference Quick CA, Watts SL, Krzyzek RA, Faras AJ. Relationship between condylomata and laryngeal papillomata. Clinical and molecular virological evidence. Ann Otol Rhinol Laryngol. 1980;89(5 Pt 1):467–71.CrossRef Quick CA, Watts SL, Krzyzek RA, Faras AJ. Relationship between condylomata and laryngeal papillomata. Clinical and molecular virological evidence. Ann Otol Rhinol Laryngol. 1980;89(5 Pt 1):467–71.CrossRef
11.
go back to reference Lynde C, Vender R, Bourcier M, Bhatia N. Clinical features of external genital warts. J Cutan Med Surg. 2013;17(Suppl 2):S55–60.PubMed Lynde C, Vender R, Bourcier M, Bhatia N. Clinical features of external genital warts. J Cutan Med Surg. 2013;17(Suppl 2):S55–60.PubMed
12.
go back to reference Wikstrom A. Clinical and serological manifestations of genital human papillomavirus infection. Acta Derm Venereol Suppl. 1995;193:1–85. Wikstrom A. Clinical and serological manifestations of genital human papillomavirus infection. Acta Derm Venereol Suppl. 1995;193:1–85.
13.
go back to reference 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.CrossRef 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.CrossRef
14.
go back to reference Chuang TY, Perry HO, Kurland LT, Ilstrup DM: Condyloma acuminatum in Rochester, Minn., 1950-1978. I. Epidemiology and clinical features. Arch Dermatol 1984, 120(4):469–475. Chuang TY, Perry HO, Kurland LT, Ilstrup DM: Condyloma acuminatum in Rochester, Minn., 1950-1978. I. Epidemiology and clinical features. Arch Dermatol 1984, 120(4):469–475.
15.
go back to reference Jeynes C, Chung MC. Challenor R: 'Shame on you'--the psychosocial impact of genital warts. Int J STD AIDS. 2009;20(8):557–60.CrossRef Jeynes C, Chung MC. Challenor R: 'Shame on you'--the psychosocial impact of genital warts. Int J STD AIDS. 2009;20(8):557–60.CrossRef
16.
go back to reference Bishai D, Kashima H, Shah K. The cost of juvenile-onset recurrent respiratory papillomatosis. Arch Otolaryngol Head Neck. 2000;126(8):935–9.CrossRef Bishai D, Kashima H, Shah K. The cost of juvenile-onset recurrent respiratory papillomatosis. Arch Otolaryngol Head Neck. 2000;126(8):935–9.CrossRef
17.
go back to reference 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.CrossRef 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.CrossRef
18.
go back to reference Castellsague X, Cohet C, Puig-Tintore LM, Acebes LO, Salinas J, San Martin M, Breitscheidel L, Remy V. Epidemiology and cost of treatment of genital warts in Spain. Eur J Pub Health. 2009;19(1):106–10.CrossRef Castellsague X, Cohet C, Puig-Tintore LM, Acebes LO, Salinas J, San Martin M, Breitscheidel L, Remy V. Epidemiology and cost of treatment of genital warts in Spain. Eur J Pub Health. 2009;19(1):106–10.CrossRef
19.
go back to reference Villa LL, Costa RL, Petta CA, Andrade RP, Ault KA, Giuliano AR, Wheeler CM, Koutsky LA, Malm C, Lehtinen M, et al. Prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase II efficacy trial. Lancet Oncol. 2005;6(5):271–8.CrossRef Villa LL, Costa RL, Petta CA, Andrade RP, Ault KA, Giuliano AR, Wheeler CM, Koutsky LA, Malm C, Lehtinen M, et al. Prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase II efficacy trial. Lancet Oncol. 2005;6(5):271–8.CrossRef
20.
go back to reference Bruni L, Diaz M, Barrionuevo-Rosas L, Herrero R, Bray F, Bosch FX, de Sanjose S, Castellsague X. Global estimates of human papillomavirus vaccination coverage by region and income level: a pooled analysis. Lancet Glob Health. 2016;4(7):e453–63.CrossRef Bruni L, Diaz M, Barrionuevo-Rosas L, Herrero R, Bray F, Bosch FX, de Sanjose S, Castellsague X. Global estimates of human papillomavirus vaccination coverage by region and income level: a pooled analysis. Lancet Glob Health. 2016;4(7):e453–63.CrossRef
21.
go back to reference Dareng EO, Adebamowo SN, Eseyin OR, Odutola MK, Pharoah PP, Adebamowo CA. Test-retest reliability of self-reported sexual behavior history in urbanized Nigerian women. Front Public Health. 2017;5:172.CrossRef Dareng EO, Adebamowo SN, Eseyin OR, Odutola MK, Pharoah PP, Adebamowo CA. Test-retest reliability of self-reported sexual behavior history in urbanized Nigerian women. Front Public Health. 2017;5:172.CrossRef
22.
go back to reference Adebamowo SN, Olawande O, Famooto A, Dareng EO, Offiong R, Adebamowo CA. Persistent low-risk and high-risk human papillomavirus infections of the uterine cervix in HIV-negative and HIV-positive women. Front Public Health. 2017;5:178.CrossRef Adebamowo SN, Olawande O, Famooto A, Dareng EO, Offiong R, Adebamowo CA. Persistent low-risk and high-risk human papillomavirus infections of the uterine cervix in HIV-negative and HIV-positive women. Front Public Health. 2017;5:178.CrossRef
23.
go back to reference Geraets DT, Struijk L, Kleter B, Molijn A, van Doorn LJ, Quint WG, Colau B. The original SPF LiPA algorithm is more sensitive and suitable for epidemiologic HPV research than the SPF INNO-LiPA extra. J Virol Methods. 2015;215:22–9.CrossRef Geraets DT, Struijk L, Kleter B, Molijn A, van Doorn LJ, Quint WG, Colau B. The original SPF LiPA algorithm is more sensitive and suitable for epidemiologic HPV research than the SPF INNO-LiPA extra. J Virol Methods. 2015;215:22–9.CrossRef
24.
go back to reference StataCorp: Stata: Release 13. In. Statistical Software. College Station, TX: StataCorp LP; 2013. StataCorp: Stata: Release 13. In. Statistical Software. College Station, TX: StataCorp LP; 2013.
25.
go back to reference 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.CrossRef 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.CrossRef
26.
go back to reference 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.CrossRef 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.CrossRef
27.
go back to reference 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.CrossRef 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.CrossRef
28.
go back to reference Fu TC, Carter JJ, Hughes JP, Feng Q, Hawes SE, Schwartz SM, Xi LF, Lasof T, Stern JE, Galloway DA, et al. Re-detection vs. new acquisition of high-risk human papillomavirus in mid-adult women. Int J Cancer. 2016;139(10):2201–12.CrossRef Fu TC, Carter JJ, Hughes JP, Feng Q, Hawes SE, Schwartz SM, Xi LF, Lasof T, Stern JE, Galloway DA, et al. Re-detection vs. new acquisition of high-risk human papillomavirus in mid-adult women. Int J Cancer. 2016;139(10):2201–12.CrossRef
29.
go back to reference Lacey CJ, Lowndes CM, Shah KV. Chapter 4: burden and management of non-cancerous HPV-related conditions: HPV-6/11 disease. Vaccine. 2006;24(Suppl 3):S3/35–41. Lacey CJ, Lowndes CM, Shah KV. Chapter 4: burden and management of non-cancerous HPV-related conditions: HPV-6/11 disease. Vaccine. 2006;24(Suppl 3):S3/35–41.
30.
go back to reference Chikandiwa A, Kelly H, Sawadogo B, Ngou J, Pisa PT, Gibson L, Didelot MN, Meda N, Weiss HA, Segondy M, et al. Prevalence, incidence and correlates of low risk HPV infection and anogenital warts in a cohort of women living with HIV in Burkina Faso and South Africa. PLoS One. 2018;13(5):e0196018.CrossRef Chikandiwa A, Kelly H, Sawadogo B, Ngou J, Pisa PT, Gibson L, Didelot MN, Meda N, Weiss HA, Segondy M, et al. Prevalence, incidence and correlates of low risk HPV infection and anogenital warts in a cohort of women living with HIV in Burkina Faso and South Africa. PLoS One. 2018;13(5):e0196018.CrossRef
31.
go back to reference Petry KU, Luyten A, Justus A, Iftner A, Strehlke S, Schulze-Rath R, Iftner T. Prevalence of low-risk HPV types and genital warts in women born 1988/89 or 1983/84 -results of WOLVES, a population-based epidemiological study in Wolfsburg. Germany BMC Infect Dis. 2012;12:367. Petry KU, Luyten A, Justus A, Iftner A, Strehlke S, Schulze-Rath R, Iftner T. Prevalence of low-risk HPV types and genital warts in women born 1988/89 or 1983/84 -results of WOLVES, a population-based epidemiological study in Wolfsburg. Germany BMC Infect Dis. 2012;12:367.
32.
go back to reference Hillman RJ, Ryait BK, Botcherby M, Taylor-Robinson D. Changes in HPV infection in patients with anogenital warts and their partners. Genitourin Med. 1993;69(6):450–6.PubMedPubMedCentral Hillman RJ, Ryait BK, Botcherby M, Taylor-Robinson D. Changes in HPV infection in patients with anogenital warts and their partners. Genitourin Med. 1993;69(6):450–6.PubMedPubMedCentral
33.
go back to reference Woodman CB, Collins S, Winter H, Bailey A, Ellis J, Prior P, Yates M, Rollason TP, Young LS. Natural history of cervical human papillomavirus infection in young women: a longitudinal cohort study. Lancet. 2001;357(9271):1831–6.CrossRef Woodman CB, Collins S, Winter H, Bailey A, Ellis J, Prior P, Yates M, Rollason TP, Young LS. Natural history of cervical human papillomavirus infection in young women: a longitudinal cohort study. Lancet. 2001;357(9271):1831–6.CrossRef
34.
go back to reference Liu P, Xu L, Sun Y, Wang Z. The prevalence and risk of human papillomavirus infection in pregnant women. Epidemiol Infect. 2014;142(8):1567–78.CrossRef Liu P, Xu L, Sun Y, Wang Z. The prevalence and risk of human papillomavirus infection in pregnant women. Epidemiol Infect. 2014;142(8):1567–78.CrossRef
35.
go back to reference 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.CrossRef 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.CrossRef
36.
go back to reference Monteiro EF, Lacey CJ, Merrick D. The interrelation of demographic and geospatial risk factors between four common sexually transmitted diseases. Sex Transm Infect. 2005;81(1):41–6.CrossRef Monteiro EF, Lacey CJ, Merrick D. The interrelation of demographic and geospatial risk factors between four common sexually transmitted diseases. Sex Transm Infect. 2005;81(1):41–6.CrossRef
37.
go back to reference Trottier H, Franco EL. The epidemiology of genital human papillomavirus infection. Vaccine. 2006;24(Suppl 1):S1–15.PubMed Trottier H, Franco EL. The epidemiology of genital human papillomavirus infection. Vaccine. 2006;24(Suppl 1):S1–15.PubMed
38.
go back to reference Dareng EO, Olaniyan Y, Adebamowo SN, Eseyin OR, Odutola MK, Obiefuna EM, Offiong RA, Pharoah PP, Adebamowo CA. Age, HIV status, and research context determined attrition in a longitudinal cohort in Nigeria. J Clin Epidemiol. 2018;100:32–43.CrossRef Dareng EO, Olaniyan Y, Adebamowo SN, Eseyin OR, Odutola MK, Obiefuna EM, Offiong RA, Pharoah PP, Adebamowo CA. Age, HIV status, and research context determined attrition in a longitudinal cohort in Nigeria. J Clin Epidemiol. 2018;100:32–43.CrossRef
39.
go back to reference Bunnell R, Mermin J, De Cock KM. HIV prevention for a threatened continent: implementing positive prevention in Africa. JAMA. 2006;296(7):855–8.CrossRef Bunnell R, Mermin J, De Cock KM. HIV prevention for a threatened continent: implementing positive prevention in Africa. JAMA. 2006;296(7):855–8.CrossRef
Metadata
Title
Prevalence and incidence of genital warts and cervical Human Papillomavirus infections in Nigerian women
Authors
Eileen O. Dareng
Sally N. Adebamowo
Ayotunde Famooto
Oluwatoyosi Olawande
Michael K. Odutola
Yinka Olaniyan
Richard A. Offiong
Paul P. Pharoah
Clement A. Adebamowo
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2019
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-018-3582-y

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