- Research article
- Open Access
- Open Peer Review
Genital warts and infection with human immunodeficiency virus in high-risk women in Burkina Faso: a longitudinal study
© Low et al; licensee BioMed Central Ltd. 2011
- Received: 3 August 2010
- Accepted: 20 January 2011
- Published: 20 January 2011
Human papillomaviruses are the most common sexually transmitted infections, and genital warts, caused by HPV-6 and 11, entail considerable morbidity and cost. The natural history of genital warts in relation to HIV-1 infection has not been described in African women. We examined risk factors for genital warts in a cohort of high-risk women in Burkina Faso, in order to further describe their epidemiology.
A prospective study of 765 high-risk women who were followed at 4-monthly intervals for 27 months in Burkina Faso. Logistic and Cox regression were used to identify factors associated with prevalent, incident and persistent genital warts, including HIV-1 serostatus, CD4+ count, and concurrent sexually transmitted infections. In a subset of 306 women, cervical HPV DNA was tested at enrolment.
Genital wart prevalence at baseline was 1.6% (8/492) among HIV-uninfected and 7.0% (19/273) among HIV-1 seropositive women. Forty women (5.2%) experienced at least one incident GW episode. Incidence was 1.1 per 100 person-years among HIV-uninfected women, 7.4 per 100 person-years among HIV-1 seropositive women with a nadir CD4+ count >200 cells/μL and 14.6 per 100 person-years among HIV-1 seropositive women with a nadir CD4+ count ≤200 cells/μL. Incident genital warts were also associated with concurrent bacterial vaginosis, and genital ulceration. Antiretroviral therapy was not protective against incident or persistent genital warts. Detection of HPV-6 DNA and abnormal cervical cytology were strongly associated with incident genital warts.
Genital warts occur much more frequently among HIV-1 infected women in Africa, particularly among those with low CD4+ counts. Antiretroviral therapy did not reduce the incidence or persistence of genital warts in this population.
- Human Immunodeficiency Virus
- Human Immunodeficiency Virus Infection
- Bacterial Vaginosis
- Genital Wart
- Human Immunodeficiency Virus Status
Human papillomaviruses (HPV) are the most common sexually transmitted infections (STI) worldwide, although they are often asymptomatic. HPV infection is usually transient, but persistence depends on HPV type and host immune status[3, 4]. HPV types are divided into high-risk (HR-HPV)and low-risk (LR-HPV), depending on their potential for causing cervical and other ano-genital cancers. The LR-HPV types HPV-6 and HPV-11 cause significant morbidity as the predominant causes of genital warts (GWs)[6, 7]. Comparatively little is known about the epidemiology and natural history of LR-HPV infection and GWs in sub-Saharan Africa. LR-HPV prevalence shows considerable regional variation, such as 11% in the Gambia, or 28% in Tanzania, and is higher among individuals infected with the human immunodeficiency virus (HIV).
HIV infection is known to alter the natural history of HPV infection. Patients co-infected with HIV-1 and HPV have a greater likelihood of HPV progression, with an increased risk for development of cervical neoplasia in immunosuppressed women. HIV-1 infected patients with GWs can experience florid and prolonged clinical manifestations driven by an impaired CD4+ T-lymphocyte response and other forms of immune dysfunction[12, 13]. Low CD4+ count (≤200 cells/μL) is the strongest independent predictor of infection with HR-HPV genotypes and is also associated with an increased risk of GWs[13, 14]. The impact of highly active antiretroviral therapy (HAART) on GWs remains uncertain, with different statistical designs revealing different effects on incidence and persistence[3, 15]. Other possibly contributing factors to GWs, such as other sexually transmitted or reproductive tract infections (STI/RTI), are poorly understood. Some studies suggest that STI/RTI increase the acquisition of HPV. However, these data are limited and predominantly from Western populations[13, 15].
We have established a cohort of women at high risk for HIV and other STI/RTI in Burkina Faso, providing an opportunity to examine the epidemiology of various STI/RTI over a three-year period. The aims of this study were to determine the prevalence, incidence and persistence of GWs, and their association with HIV infection, immunosuppression, and other risk factors in an African setting.
Participants and study procedures
The Yérélon Cohort was established in 1998 to examine factors associated with HIV infection among professional female sex workers and other high-risk women in Burkina Faso and to design interventions to prevent infection. A new phase of enrolment began in December 2003 and continued until January 2005. Women were eligible for enrolment if they declared a history of at least one transactional sex act per week, were aged 16 years or older, and were willing to undergo HIV testing. Some women were recruited from local organizations for people living with HIV/AIDS, using the same criteria. All women provided written informed consent. The Yérélon Cohort research protocol was approved by the institutional review board at Centre Muraz, and the research ethics committees at the Burkina Faso Ministry of Health and the London School of Hygiene & Tropical Medicine.
Participants were followed approximately every 4 months until February 2006 for a maximum of 6 follow-up visits. At enrolment, an interviewer administered a questionnaire eliciting socio-demographic and behavioral characteristics, and sexual health information. At subsequent visits, intervening behavioral, sexual health and treatment information was collected. At all visits a study clinician performed a full physical exam and collected genital samples. Clinicians documented the presence of abnormal discharge, genital ulcers, and GWs, which were defined as a genital proliferation with the clinical appearance of condylomata acuminata. The genital sites were described as the cervix, vagina, labia, or 'external' (outer pubic and anal) areas. Patients were treated for STI/RTI according to national guidelines; there was no treatment available for GWs. Since April 2004, HIV-infected participants meeting the World Health Organization (WHO) eligibility criteria for HAART initiation in developing countries have been provided with antiretrovirals. Women with HIV clinical stages III or IV or with a CD4+ count ≤200 cells/μL were treated with standard antiretroviral therapy, primarily zidovudine (AZT), lamivudine (3TC) and efavirenz (EFV). Women already on HAART at the enrolment visit had been provided with medications at the Bobo-Dioulasso University Hospital.
Vaginal smears were examined using wet-mount microscopy to detect Trichomonas vaginalis (TV) and Gram-stained to diagnose bacterial vaginosis (BV). Diagnosis of Neisseria gonorrhoeae was made by culture of cervical swabs using modified Thayer-Martin media. Chlamydia trachomatis diagnosis could not be performed during the study, but has been shown to be rare in this population.
Blood samples were collected at enrolment and then every 4 months. Syphilis serostatus was determined every 12 months using the rapid plasma reagin test (RPR, Human GmbH) confirmed with a Treponema pallidum haemagglutination assay (TPHA, Newmarket Laboratories). HSV-2 serology was done using the Kalon IgG2-ELISA test (Kalon Biologicals). HIV serology was done at enrolment and every 4 months among seronegative women using a Determine-1/2 rapid testing kit (Abbott Laboratories) with Genie-II (Bio-Rad Laboratories) confirmation. CD4+ counts were determined using FACScan (Becton Dickinson) at enrolment and every 6 months among HIV-1 seropositive women; plasma HIV-1 RNA was quantified every 6 to 12 months using real-time PCR with a lower limit of detection of 300 (2.48 log10 ) copies/mL. Values were converted to log10 copies/mL; those below the threshold of detection were assigned a value of half the threshold.
A subset of women enrolled between December 2003 and March 2004 submitted an additional cervical swab at enrolment for HPV DNA detection and liquid-based cytology using a Cervex swab and the ThinPrep 2000 processor (Cytyc Corporation). HPV genotyping was performed using the INNO-LiPA genotyping v2 test (Innogenetics). The 2001 Bethesda classification was used for Papanicolaou-stained cervical slides interpretation.
Prevalent GWs were defined as the presence of clinically-defined condylomata acuminata at the enrolment visit. Due to the small number of women with CD4+ counts at the enrolment visit, women were classified as HIV seronegative and HIV-1 seropositive at baseline. Incident GWs were defined as the first documented occurrence of condylomata acuminata in a previously undocumented site after the enrolment visit. Women with a GW in one location who developed a lesion in a new location were included as a new incident event. Persistent GWs were defined as GWs present in the same anatomical site for at least two consecutive visits, which could include the enrolment visit. Women were stratified during study follow-up according to their nadir CD4+ count in the following categories: (i) HIV-negative, (ii) HIV-1 positive with a nadir CD4+ count >200 cells/μL, and (iii) HIV-1 positive with a nadir CD4+ count ≤200 cells/μL.
Analyses examined the association between HIV status and other potential risk factors with prevalent GWs. Univariate associations were examined using chi-squared tests for categorical variables and two-sample t-tests for continuous variables. Due to the strong associations between many of our variables of interest, a multivariate logistic regression model was developed in a stepwise fashion including HIV status and risk factors either decided a priori or independently associated with prevalent GWs using p < 0.05 as the inclusion criterion.
We measured incidence and persistence of GWs and determined associations of potential risk factors with these outcomes using Cox regression. To allow for intra-subject correlation, these models used shared frailty. Other potential risk factors included time-updated measures, such as concurrent STI/RTI, use of HAART, and behavioral measures recorded at follow-up visits. In order to establish the most likely ordering of events, measures of behavior and confirmed STI/RTI over the preceding period were taken from the visit at which incident or persistent GWs were identified and serological time-updated measures were taken from the visit preceding any visit at which a new GW was identified. For HIV-1 seropositive women, a separate model was constructed which included CD4+ count and HAART use at the prior visit and maximum viral load during the study period. Nadir CD4+ count was not included in these models because model convergence could not be achieved.
Further analyses were conducted to examine the association of cervical HPV and squamous intraepithelial lesions (SIL) with incident GWs among women from whom cervical HPV DNA had been collected, using the same methods as above to construct the final model.
The effect of time in the study was assessed for each variable in all models and an interaction parameter was included if the hazard ratio changed significantly after one year of follow-up.
Statistical analyses were performed using Stata version10.0 (StataCorp).
Characteristics of cohort participants
Characteristics of 765 high-risk women at cohort enrolment, according to HIV-1 serostatus
HIV seronegative (N = 492) n (%)
HIV-1 seropositive (N = 273) n (%)
Age groups, years (N = 759)
Education (N = 752)
Primary or above
Marital status (N = 754)
Age at first sex, median (IQR), years
Number of sex partners in last week (N = 752)
Currently smoking (N = 759)
Contraceptive use (N = 760)
Practices regular vaginal douching
Condom use with clients/partners (N = 751)
Current genital warts
Bacterial vaginosis (N = 718)
Trichomonas vaginalis (N = 596)
HSV-2 positive serology (N = 689)
Current antiretroviral therapy (HAART)
CD4+ count, cells/μL :
Not on HAART (N = 242)
On HAART (N = 25)
Plasma HIV-1 RNA, log10 copies/mL d:
Not on HAART (N = 233)
On HAART (N = 24)
Cervical HPV-6 or -11 (N = 306)f
LSIL (N = 306)f
HSIL (N = 306)f
In the analysis of the 306 women from whom cervical cytological samples were collected, HIV-1 seropositive women had significantly more cervical squamous intraepithelial lesions than HIV-uninfected women (P < 0.001) (Table 1). There were no cases of atypical squamous cells-cannot exclude HSIL (ASC-H), atypical glandular cells (AGC), or cancer identified.
Prevalent genital warts and associated risk factors
At enrolment, 27 women (3.5%) had GWs, 1.6% (8/492) among HIV-uninfected and 7.0% (19/273) among HIV-1 seropositive women (P < 0.001) (Table 1). There were no prevalent GWs among the 26 women taking HAART. In the multivariate analysis, which included HSV-2 serostatus, the presence of bacterial vaginosis, number of recent sexual partners and age group, there was a 5-fold increase in risk for prevalent GWs in HIV-1 seropositive women (adjusted odds ratio [aOR] 5.33, 95%CI: 1.97 to 14.40, P = 0.001). Women who smoked had a 3-fold increased risk of prevalent GW (aOR 3.55, 95%CI: 1.03 to 12.32, P = 0.05). For HIV-1 seropositive women, there was no evidence of a relationship between CD4+ count and prevalence of GWs (CD4+ count >200 cells/μL vs. ≤200 cells/μL, [aOR = 1.77, 95%CI: 0.36 to 8.61, P = 0.48). None of the other variables shown in Table 1 were associated with prevalent GWs.
Incident genital warts and associated risk factors
Over the 27 months of the study, 16.9% (129/765) of women were lost to follow-up. Twenty-one women died, all of whom were HIV-1 seropositive. The percentage of scheduled visits attended was 83.3%; this did not differ by HIV-1 serostatus.
Univariate and multivariate assessment of factors associated with incident genital warts over three years
Number of events/person-years
Unadjusted HRa(95% CI)
Adjusted HRb(95% CI)
1. Among all women:
HIV status, nadir CD4+ count
HIV-1+, CD4 >200cells/μL
HIV-1+, CD4 ≤200 cells/μL
Age groups, years
Age at first sex, years
HSV-2 positive serology
History of pregnancy
Number of sex partners in past week
Practices regular vaginal douching
Condom use with clients/partners
Days since last menstruationc
2. Among HIV-1 positive women only:
On HAART at prior visit
Highest log10 viral load in the past 3 years
CD4+ count at prior visit (per 100 cells/μL increase)
In the multivariate model including all women, HIV-1 and nadir CD4+ count were the strongest predictors of incident GWs. Compared to HIV-uninfected women, HIV-1-seropositive women with a nadir CD4+ ≤200 cells/μL had an almost 20-fold higher risk of incident GWs (adjusted hazard ratio [aHR] 19.13, 95%CI: 6.94 to 52.71, P < 0.001); among HIV-1-seropositive women with CD4+ counts >200 cells/μL, the estimated risk was 6-fold higher (aHR 6.51, 95%CI: 2.38 to 17.78, P < 0.001). Having a primary education or above was protective (aHR 0.45, 95%CI: 0.23 to 0.88, P = 0.02). For the time-updated variables, concurrent bacterial vaginosis (aHR 2.17, 95%CI: 1.13 to 4.18, P = 0.02), and genital ulceration (aHR 3.29, 95%CI: 1.13 to 9.55, P = 0.03) were associated with incident GWs.
The model among HIV-1 seropositive women indicated a trend towards a protective effect for increasing CD4+ count at the prior visit (aHR 0.79 for each 100 cells/μL increase, 95%CI: 0.61 to 1.02, P = 0.07), but the use of HAART per se was not protective. High maximum HIV-1 plasma viral load was predictive of incident GWs, although this was not statistically significant. There was no evidence of an interaction between nadir CD4+ count and time since enrolment on incidence of GWs.
Persistence of genital warts
In the absence of treatment, 40% of women with an identified GW (16/40) had persistent warts at the next visit. The strongest predictor of GW persistence was HIV-1 status and nadir CD4+ count: GW persistence was 0.4 per 100 person-years among HIV-uninfected women, 6.1 per 100 person-years among HIV-1 seropositive women with nadir CD4+ counts >200 cells/μL, and 13.4 per 100 person-years for those women with nadir CD4+ counts ≤200 cells/μL. The multivariate model among HIV-1 seropositive women indicated that there was no protective effect of prior antiretroviral treatment on persistence (aHR 1.71, 95%CI: 0.40 to 7.23, P = 0.47), but there was weak evidence that a CD4+ count was protective (aHR 0.72 for each 100 cells/μL increase, 95%CI: 0.45 to 1.14, P = 0.16). No other factors were significantly associated with persistence of GWs.
Association of HPV-6 or -11 with incident genital warts
Associations between cervical HPV DNA, HIV-1 serostatus and cytology and incident genital warts among a sub-group of 306 women
Number of events/person-years
Unadjusted HRa(95% CI)
Adjusted HRb(95% CI)
Cervical HPV DNA at baseline
HPV-6 positive, yes vs. no
Effect in 1st year of follow-up
Effect after 1st year of follow-up
HPV-11 positive, yes vs. no
HPV-52 positive, yes vs. no
Other HPV types, negative for types 6, 11,52
Cervical cytology at baseline (N = 296)
HIV status, nadir CD4+ count
HIV-1+, CD4 >200cells/μL
HIV-1+, CD4 ≤200 cells/μL
This study provides the first longitudinal data on the natural history of GWs among HIV infected women in Africa. In this setting, we found an overall prevalence of GWs of 3.5%. This is consistent with GW prevalence from other countries in Africa, although this depends on the region, prevalence of HIV-1, and the sexual risk behaviours of studied populations. The Women's Interagency HIV Study in the USA reported GW incidences of 2.2 per 100 person-years in HIV-uninfected and 8.9 per 100 person-years in HIV-1 seropositive women, which are similar to our findings .
As in studies in developed countries, HIV-1 infection and immune function, as measured by nadir CD4+ count, were the most powerful predictors of incident and persistent GWs,[13, 15] even after adjusting for the presence of HPV. Although only partially understood, GW regression is thought to be dependent upon the cell-mediated immune response; CD4+ T-lymphocytes have been shown to be present in large numbers in the stroma under the lesions and in the regressing warts themselves, but their role in clearance has not been entirely elucidated[12, 25]. In studies of canine oral papillomavirus, it is the response of CD4+ cells to viral proteins E6 and E7 that is responsible for regression of lesions. The strong association between concurrent BV and genital ulceration and incident GWs supports a common determinant. There is good evidence supporting the role of the vaginal flora in both susceptibility to and clearance of infections, as HPV infects via micro-abrasions in the genital mucosa.
This is the first study to evaluate the impact of HAART on GWs in women in Africa. We did not detect any protective effect of HAART on incidence or persistence, despite the overall excellent adherence achieved in this cohort. The burden of HR-HPV was recently shown to be reduced by effective HAART, but the impact on LR-HPV is unknown, and its effect on GWs varies between studies[3, 15]. However, our interpretation of these results is limited by the relatively small number of visits for women on HAART, and the partial data on concurrent CD4+ count and HIV-1 viral loads.
We identified a strong association between detection of cervical HPV-6 DNA and incident GWs in the first year of follow-up. Our data also support studies demonstrating a relative lack of epidemiological contribution of HPV-11 in GWs[7, 30]. HPV-52 has been identified as one of the types most commonly identified in GWs in conjunction with HPV-6 in Australia. Furthermore, a study of HPV in GWs in France demonstrated that 6.4% of patients with GWs had HPV-52 on cytobrush sampling. It is probable that cervical HPV was only partially representative of causative genotypes for GWs; the trend towards an increase in GWs in women infected with other types of HPV could reflect local but undetected infection with HPV-6 or 11. Furthermore, the small number of women infected with HPV-11 limits the power of this study to detect an association. However, as there are few studies examining the distribution of HPV in GWs in Africa, it is possible that this reflects a different epidemiology of HPV in this region compared to other settings. Further studies with larger numbers of women and direct sampling of warts for HPV types are required to better understand this relationship.
Study limitations include the varying time between visits, and the broad categorization of anatomical location which might have led to undetected new GWs and thus an underestimate of incidence. Although rare in this setting, it is also possible that some women sought treatment for GWs elsewhere, which may have resulted in underestimates of GW persistence.
This is the first study to examine the natural history of genital warts in African women and the impact of HIV-1 infection and HAART. This high-risk population with high HIV prevalence and GW incidence and little access to ablative therapy may contribute more to HPV transmission and suffer disproportionately from the consequences of HPV infection. We have demonstrated a high incidence of genital warts in this population, and a very strong association with immune suppression from HIV-1 infection; there was no protective effect from HAART. This and other epidemiological studies of HPV types in different populations should inform further vaccine development designed for African women.
This study was funded by France's Agence Nationale de Recherches sur le SIDA et les Hépatites (ANRS). Additional financial support was provided through the UK's Department for International Development (DFID)-funded Knowledge Programme on HIV/AIDS & STI and the Research Programme Consortium on Research and Capacity Building in Sexual & Reproductive Health and HIV in Developing Countries.
We wish to thank the women and the organisations of persons living with HIV/AIDS ('Yérelon', 'Espoir et Vie', Centre 'Solidarité Action Sociale' and 'Espoir pour Demain') who participated in this study; and staff at Service d'Hygiène, Bobo-Dioulasso, Burkina Faso. We also wish to thank Professor Charles Lacey (Hull York Medical School, York, UK) for his critical evaluation of this manuscript.
* Composition of the Yérelon study group
Eloi Bahembera, Abdramane Berthée, Minata Coulibaly, Marie-Christine Defer, Ramata Diallo, Didier Djagbaré, Charlotte Huet, Issouf Konaté, Florent Ky-Dama, Gilles T. M'Boutiki, Nicolas Méda, Inès Millogo, Nicolas Nagot, Abdoulaye Ouédraogo, Djénéba Ouédraogo, Francois Rouet, Anselme Sanon, Haoua Sawadogo, Roselyne Vallo, and Laurence Vergne [deceased January 2007] (Centre Muraz, Bobo-Dioulasso, Burkina Faso); Philippe Mayaud, Nicolas Nagot, and Helen A. Weiss (London School of Hygiene and Tropical Medicine, London, UK); Pierre Becquart, Vincent Foulongne, Michel Segondy, and Philippe Van de Perre, (Université Montpellier 1, and CHU Montpellier, Montpellier, France); Jean-Baptiste Andonaba and Adrien Sawadogo (University Hospital of Bobo-Dioulasso, Burkina Faso).
- Burchell AN, Winer RL, de Sanjose S, Franco EL: Chapter 6: Epidemiology and transmission dynamics of genital HPV infection. Vaccine. 2006, 24 (Suppl 3): S52-61. 10.1016/j.vaccine.2006.05.031.View ArticleGoogle Scholar
- Ho GY, Bierman R, Beardsley L, Chang CJ, Burk RD: Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med. 1998, 338: 423-428. 10.1056/NEJM199802123380703.View ArticlePubMedGoogle Scholar
- Massad LS, Silverberg MJ, Springer G, Minkoff H, Hessol N, Palefsky JM, Strickler HD, Levine AM, Sacks HS, Moxley M, Heather Watts D: Effect of antiretroviral therapy on the incidence of genital warts and vulvar neoplasia among women with the human immunodeficiency virus. Am J Obstet Gynecol. 2004, 190: 1241-1248. 10.1016/j.ajog.2003.12.037.View ArticlePubMedGoogle Scholar
- 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: 37-45. 10.1086/421467.View ArticlePubMedGoogle Scholar
- Roman A, Fife KH: Human papillomaviruses: are we ready to type?. Clin Microbiol Rev. 1989, 2: 166-190.View ArticlePubMedPubMed CentralGoogle Scholar
- Aubin F, Pretet JL, Jacquard AC, Saunier M, Carcopino X, Jaroud F, Pradat P, Soubeyrand B, Leocmach Y, Mougin C, Riethmuller D: Human papillomavirus genotype distribution in external acuminata condylomata: a Large French National Study (EDiTH IV). Clin Infect Dis. 2008, 47: 610-615. 10.1086/590560.View ArticlePubMedGoogle Scholar
- Garland SM, Steben M, Sings HL, James M, Lu S, Railkar R, Barr E, Haupt RM, Joura EA: Natural history of genital warts: analysis of the placebo arm of 2 randomized phase III trials of a quadrivalent human papillomavirus (types 6, 11, 16, and 18) vaccine. J Infect Dis. 2009, 199: 805-814. 10.1086/597071.View ArticlePubMedGoogle Scholar
- Wall SR, Scherf CF, Morison L, Hart KW, West B, Ekpo G, Fiander AN, Man S, Gelder CM, Walraven G, Borysiewicz LK: Cervical human papillomavirus infection and squamous intraepithelial lesions in rural Gambia, West Africa: viral sequence analysis and epidemiology. Br J Cancer. 2005, 93: 1068-1076. 10.1038/sj.bjc.6602736.View ArticlePubMedPubMed CentralGoogle Scholar
- Mayaud P, Gill DK, Weiss HA, Uledi E, Kopwe L, Todd J, ka-Gina G, Grosskurth H, Hayes RJ, Mabey DC, Lacey CJ: The interrelation of HIV, cervical human papillomavirus, and neoplasia among antenatal clinic attenders in Tanzania. Sex Transm Infect. 2001, 77: 248-254. 10.1136/sti.77.4.248.View ArticlePubMedPubMed CentralGoogle Scholar
- Didelot-Rousseau MN, Nagot N, Costes-Martineau V, Valles X, Ouedraogo A, Konate I, Weiss HA, Van de 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: 355-362. 10.1038/sj.bjc.6603252.View ArticlePubMedPubMed CentralGoogle Scholar
- Chaturvedi AK, Madeleine MM, Biggar RJ, Engels EA: Risk of human papillomavirus-associated cancers among persons with AIDS. J Natl Cancer Inst. 2009, 101: 1120-1130. 10.1093/jnci/djp205.View ArticlePubMedPubMed CentralGoogle Scholar
- Lacey CJ: Therapy for genital human papillomavirus-related disease. J Clin Virol. 2005, 32 (Suppl 1): S82-90. 10.1016/j.jcv.2004.10.020.View ArticlePubMedGoogle Scholar
- 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: 427-435. 10.1097/00007435-200208000-00001.View ArticlePubMedGoogle Scholar
- 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: 403-409. 10.1016/S0029-7844(00)00948-0.PubMedGoogle Scholar
- Dolev JC, Maurer T, Springer G, Glesby MJ, Minkoff H, Connell C, Young M, Schowalter K, Cox C, Hessol NA: Incidence and risk factors for verrucae in women. AIDS. 2008, 22: 1213-1219. 10.1097/QAD.0b013e3283021aa3.View ArticlePubMedPubMed CentralGoogle Scholar
- World Health Organization. Dept. of HIV/AIDS. Interim WHO Antiretroviral Treatment Working Group: Scaling up antiretroviral therapy in resource-limited settings : guidelines for a public health approach. 2002, Geneva: World Health OrganizationGoogle Scholar
- Nugent RP, Krohn MA, Hillier SL: Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol. 1991, 29: 297-301.PubMedPubMed CentralGoogle Scholar
- Nagot N, Ouedraogo A, Ouangre A, Cartoux M, Defer MC, Meda N, Van de Perre P: Is sexually transmitted infection management among sex workers still able to mitigate the spread of HIV infection in West Africa?. J Acquir Immune Defic Syndr. 2005, 39: 454-458. 10.1097/01.qai.0000152399.54648.b9.View ArticlePubMedGoogle Scholar
- Rouet F, Chaix ML, Nerrienet E, Ngo-Giang-Huong N, Plantier JC, Burgard M, Peeters M, Damond F, Ekouevi DK, Msellati P, et al: Impact of HIV-1 genetic diversity on plasma HIV-1 RNA Quantification: usefulness of the Agence Nationale de Recherches sur le SIDA second-generation long terminal repeat-based real-time reverse transcriptase polymerase chain reaction test. J Acquir Immune Defic Syndr. 2007, 45: 380-388. 10.1097/QAI.0b013e3180640cf5.View ArticlePubMedGoogle Scholar
- Didelot-Rousseau MN, Courgnaud V, Nagot N, Ouedraogo A, Konate I, Mayaud P, Weiss H, Van de Perre P, Segondy M: Comparison of INNO-LiPA HPV Genotyping v2 with PCR product subcloning and sequencing for identification of genital human papillomavirus genotypes in African women. J Virol Methods. 2006, 135: 181-185. 10.1016/j.jviromet.2006.03.015.View ArticlePubMedGoogle Scholar
- Smith JH: Bethesda 2001. Cytopathology. 2002, 13: 4-10. 10.1046/j.1365-2303.2002.00397.x.View ArticlePubMedGoogle Scholar
- Xue X, Gange SJ, Zhong Y, Burk RD, Minkoff H, Massad LS, Watts DH, Kuniholm MH, Anastos K, Levine AM, et al: Marginal and mixed-effects models in the analysis of human papillomavirus natural history data. Cancer Epidemiol Biomarkers Prev. 2010, 19: 159-169. 10.1158/1055-9965.EPI-09-0546.View ArticlePubMedPubMed CentralGoogle Scholar
- Low A, Didelot-Rousseau MN, Nagot N, Ouedraougo A, Clayton T, Konate I, Van de Perre P, Segondy M, Mayaud P: Cervical infection with human papillomavirus (HPV) 6 or 11 in high-risk women in Burkina Faso. Sex Transm Infect. 2010Google Scholar
- Mayaud P, Weiss HA, Lacey CJ, Gill DK, Mabey DC: Genital human papillomavirus genotypes in northwestern Tanzania. J Clin Microbiol. 2003, 41: 4451-4453. 10.1128/JCM.41.9.4451-4453.2003.View ArticlePubMedPubMed CentralGoogle Scholar
- Hong K, Greer CE, Ketter N, Van Nest G, Paliard X: Isolation and characterization of human papillomavirus type 6-specific T cells infiltrating genital warts. J Virol. 1997, 71: 6427-6432.PubMedPubMed CentralGoogle Scholar
- Jain S, Moore RA, Anderson DM, Gough GW, Stanley MA: Cell-mediated immune responses to COPV early proteins. Virology. 2006, 356: 23-34. 10.1016/j.virol.2006.07.032.View ArticlePubMedGoogle Scholar
- Watts DH, Fazzari M, Minkoff H, Hillier SL, Sha B, Glesby M, Levine AM, Burk R, Palefsky JM, Moxley M, et al: Effects of bacterial vaginosis and other genital infections on the natural history of human papillomavirus infection in HIV-1-infected and high-risk HIV-1-uninfected women. J Infect Dis. 2005, 191: 1129-1139. 10.1086/427777.View ArticlePubMedGoogle Scholar
- Huet C, Ouedraogo A, Konate I, Traore I, Rouet F, Ouiminga A, A S, Mayaud P, Van de Perre P, Nagot N: Feasibility and efficacy of highly active antiretroviral therapy among high-risk and marginalised HIV-1 infected women in West Africa. Book Feasibility and efficacy of highly active antiretroviral therapy among high-risk and marginalised HIV-1 infected women in West Africa. 2009, CityGoogle Scholar
- Minkoff H, Zhong Y, Burk RD, Palefsky JM, Xue X, Watts DH, Levine AM, Wright RL, Colie C, D'Souza G, et al: Influence of adherent and effective antiretroviral therapy use on human papillomavirus infection and squamous intraepithelial lesions in human immunodeficiency virus-positive women. J Infect Dis. 2010, 201: 681-690. 10.1086/650467.View ArticlePubMedPubMed CentralGoogle Scholar
- Vandepapeliere P, Barrasso R, Meijer CJ, Walboomers JM, Wettendorff M, Stanberry LR, Lacey CJ: Randomized controlled trial of an adjuvanted human papillomavirus (HPV) type 6 L2E7 vaccine: infection of external anogenital warts with multiple HPV types and failure of therapeutic vaccination. J Infect Dis. 2005, 192: 2099-2107. 10.1086/498164.View ArticlePubMedGoogle Scholar
- The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2334/11/20/prepub
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.