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Prevalence of Anal High-Risk Human Papillomavirus Infections Among HIV-Positive and HIV-Negative Men Who Have Sex With Men in Nigeria

Nowak, Rebecca G. PhD; Gravitt, Patti E. PhD; He, Xin PhD; Ketende, Sosthenes MSc; Dauda, Wuese MBBS; Omuh, Helen MBBS MS; Blattner, William A. MD; Charurat, Manhattan E. PhD on behalf of the TRUST Study Group

Sexually Transmitted Diseases: April 2016 - Volume 43 - Issue 4 - p 243–248
doi: 10.1097/OLQ.0000000000000431
Original Study

Background Prevalence estimates of anal high-risk human papillomavirus (HR-HPV) are needed in sub-Saharan Africa where HIV is endemic. This study evaluated anal HR-HPV in Nigeria among HIV-positive and HIV-negative men who have sex with men (MSM) for future immunization recommendations.

Methods We conducted a cross-sectional study to compare the prevalence of anal HR-HPV infections between 64 HIV-negative and 90 HIV-positive MSM. Multivariate Poisson regression analyses were used to examine demographic and behavioral risk factors associated with any HR-HPV infections.

Results The median age of the 154 participants was 25 years (interquartile range, 22–28 years; range, 16–38 years), and the median age at initiation of anal sex with another man was 16 years (interquartile range, 13–18 years; range, 7–29 years). The prevalence of anal HR-HPV was higher among HIV-positive than HIV-negative MSM (91.1% vs. 40.6%, P < 0.001). In the multivariate analysis, HIV infection (adjusted prevalence ratio [aPR], 2.02; 95% confidence interval [CI], 1.49–2.72), 10 years or more since anal sexual debut (aPR, 1.26; 95% CI, 1.07–1.49), and concurrent relationships with men (aPR, 1.32; 95% CI, 1.04–1.67) were associated with increased anal HR-HPV prevalence.

Conclusions Anal HR-HPV infection is high for young Nigerian MSM, and rates are amplified in those coinfected with HIV. Providing universal coverage as well as catch-up immunization for young MSM may be an effective anal cancer prevention strategy in Nigeria.

Young HIV-positive men who have sex with men from Nigeria have a 2-fold higher prevalence of anal human papillomavirus as compared with HIV-negative men.

From the *Institute of Human Virology and †Department of Epidemiology and Public Health, University of Maryland School of Medicine, Baltimore, MD; ‡University of New Mexico Health Sciences Center, Albuquerque, NM; §University of Maryland School of Public Health, College Park, MD; ¶Johns Hopkins Bloomberg School of Public Health, Baltimore, MD; and ∥Institute of Human Virology Nigeria, Federal Capital Territory, Nigeria

Acknowledgments: The authors thank the participants and the TRUST study team. They also thank Rex Lin, Brian Taylor, Damon Getman, and Alice Jiang in their assistance with DNA extractions as well as Dr Maura Gillison and Weihong Xiao for conducting the human papillomavirus genotyping.

The TRUST Study Group is constituted as follows:

Principal investigators: William Blattner and Man Charurat (Institute of Human Virology, University of Maryland, Baltimore, MD).

Co-investigators: Alash'le Abimiku, Sylvia Adebajo, Julie Ake, Stefan Baral, Trevor Crowell, Charlotte Gaydos, Lindsay Hughes, Babajide Keshinro, Jerome Kim, Hongjie Liu, Jennifer Malia, Nelson Michael, Ogbonnaya Njoku, Rebecca Nowak, Helen Omuh, Ifeanyi Orazulike, Sheila Peel, Merlin Robb, Cristina Rodriguez-Hart, Sheree Schwartz.

Institutions: Institute of Human Virology at the University of Maryland School of Medicine, Johns Hopkins Bloomberg School of Public Health; Walter Reed Army Institute of Research; US Military HIV Research Program; Department of Defense; Walter Reed Program, Nigeria; Institute of Human Virology Nigeria; International Centre for Advocacy for the Right to Health; Population Council.

Conflicts of interest: None of the authors have conflicts of interest to declare.

Funding sources: The research reported in this publication was supported by the US National Institutes of Health under award number R01MH099001-01. This study is also supported by funds from the University of Maryland, School of Medicine, Department of Epidemiology and Public Health (seed funding), the US Military HIV Research Program (Grant No. W81XWH-07-2-0067), Fogarty AITRP (D43TW01041), and the President's Emergency Plan for AIDS Relief through cooperative agreement U2G IPS000651 from the HHS/Centers for Disease Control and Prevention, Global AIDS Program with Institute of Human Virology Nigeria. The content is solely the responsibility of the authors and does not necessarily represent the official views of the Department of Defense, National Institutes of Health, or other funders.

Correspondence: Rebecca Nowak, PhD, Institute of Human Virology, University of Maryland School of Medicine, 725 W. Lombard St, Baltimore, MD 21201. E-mail:

Received for publication August 4, 2015, and accepted December 28, 2015.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text, and links to the digital files are provided in the HTML text of this article on the journal's Web site (

The rising incidence of anal cancer in the United States is linked to the syndemic of HIV and coincident high-risk human papillomavirus (HR-HPV) infection among men who have sex with men (MSM). Anal cancer risk is 80 times higher among HIV-infected MSM as compared with HIV-uninfected individuals, with the most oncogenic genotypes being HPV16 followed by HPV18 and HPV33.1–3 Antiretroviral therapy (ART) has restored systemic immunity, but has done little to regress anal precancerous lesions4,5 or prevent an increase in anal cancer incidence in HIV-positive men.1,6,7 These unexpected trends in the era of ART highlight the complexity of HPV transformation and the need to prevent initial infection with effective HPV vaccines.

Most prevalence studies of anal HR-HPV in HIV-infected MSM have occurred in North America, Europe, Australia, and Asia.8–14 A meta-analysis of cross-sectional studies primarily from the United States estimated that the pooled prevalence of any HPV was higher in HIV-positive as compared with HIV-negative MSM (93% vs. 64%).15 A similar pattern existed for HR-HPV (74% vs. 37%).15 More data are needed to describe the burden of anal HR-HPV in HIV-endemic regions such as sub-Saharan Africa for adequate anal cancer control program development. This is especially important because with longer survival times expected for HIV-infected populations in sub-Saharan Africa, anal cancer trends are likely to parallel and possibly surpass the current trends seen in the United States, where the incidence rates among men increased between 2000 and 2009.6 The 9-valent HPV vaccine which includes protection against 5 additional HR-HPV types (31, 33, 45, 52, and 58) was recently approved in December 2014 by the US Food and Drug Administration for boys between the ages of 9 to 15 years.16 The anticipated impact of the 9-valent HPV vaccine on anal HPV burden is difficult to estimate in an HIV endemic area such as Nigeria, where the diversity of HR-HPV has not been characterized.

The objective of this study is, thus, to evaluate the prevalence of anal HR-HPV and associated demographic and behavioral risk factors in a cohort of young HIV-positive and HIV-negative Nigerian MSM to better inform future vaccination recommendations.

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Study Design and Population

We conducted a cross-sectional study at the Abuja site of the TRUST study that has been previously described.17 In brief, the TRUST study has recruited Nigerian MSM through respondent-driven sampling (RDS) since March 2013. Eligibility criteria included the following: (1) a valid RDS coupon; (2) born male; (3) history of anal intercourse, insertive, or receptive, with another man in the past 12 months; (3) 16 years or older, with 16- to 17-year-olds considered emancipated minors and exempt from parental consent; and (4) ability and willingness to provide written informed consent. At enrollment (visit 0), participants provided demographic, sexual behavior, and clinical data through in-person interviews by the trained staff using a standardized questionnaire. Two weeks after enrollment (visit 1), participants underwent HIV counseling and testing and received physical examinations where anal swabs, urine, and blood were collected for sexually transmitted infection (STI) diagnostics. Two anal swabs from the APTIMA swab kit were inserted by a doctor approximately 2 cm into the anorectum, rotated, and placed in transport medium. Specimens were aliquoted and stored at −80°C before testing. At the time of this analysis, participants who had completed HIV testing, had an anal swab sample at visit 1, and were among those recruited early in the TRUST study by their peers (waves 1–10 of network chains) were included in this study (n = 165).

This study was conducted in collaboration with the Institute of Human Virology at the University of Maryland, the Institute of Human Virology Nigeria, Johns Hopkins University, the International Center for Advocacy on the Right to Health, and the US Military HIV Research Program. The study was approved by the Federal Capital Territory Health Research Ethics Committee in Nigeria, the University of Maryland Baltimore Institutional Review Board, and the Walter Reed Army Institute of Research Institutional Review Board.

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Laboratory Procedures

Whole blood was tested for HIV using rapid test kits (Abbott Determine HIV-1/2, Chembio HIV-1/2 Stat Pak, and Trinity biotech Uni-Gold HIV test for discordant results) as outlined by the parallel testing algorithm for high-risk individuals in Nigeria.18 If a participant was HIV positive, HIV RNA viral loads were quantified using the COBAS TaqMan HIV-1 Test (Roche Molecular Diagnostics, Pleasanton, CA) and CD4 counts were estimated using the Partec CyFlow Counter. Anal swabs were tested for Neisseria gonorrhoeae and Chlamydia trachomatis using the Aptima Combo 2 CT/NG Assay (Hologic, San Diego, CA). Participants testing positive for HIV and/or STIs were offered ART regardless of CD4 counts and antibiotic therapies. A physical examination of the anorectum was conducted for detection of warts. Depending on the size of the warts, the participants were either treated with liquid nitrogen immediately or referred to the Nigerian Defense Headquarters Medical Center for surgical excision.

For HPV analyses, DNA was extracted from 250 μL of Aptima Specimen Transport medium using the QIAamp MinElute Media Kit (Qiagen, Valencia, CA). DNA was resuspended in 100 μL of Buffer AVE. A 10-μL aliquot of the purified DNA was amplified using the PGMY 09/11 L1 consensus primer system19 which co-amplifies 37 HPV genotypes and a human β-globin internal control target. Both high- and low-risk HPV genotypes were detected using the Linear Array HPV Genotyping Test (Roche Molecular Diagnostics).20 High-risk HPV included 13 type specific infections: 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, and 68.21 HPV52 was considered positive if there was no cross-reaction with HPV33, HPV35, or HPV58. HPV52 status in men with HPV33, HPV35, or HPV58 is therefore unknown. The remaining 24 genotypes detected were considered low risk. Quality control samples were included during DNA extraction, polymerase chain reaction amplification, and genotype detection steps. Among the 165 samples tested, 8 were excluded from the analysis because they did not have sufficient cellular material to detect HPV genotypes. The final analytic sample size was 157.

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Statistical Analyses

The primary outcome variable for all analyses was a binary categorization of having any anal HR-HPV type-specific infections. A person was considered positive if 1 or more of the 13 HR-HPVs was detected. Prevalence of any HPV, vaccine-preventable types in the 9-valent vaccine (HPV6, 11, 16, 18, 31, 33, 45, 52, 58), HR-HPV not in the 9-valent vaccine (HPV35, 39, 51, 56, 59, 68), and individual high-risk type specific infections between HIV-positive and HIV-negative were also assessed. The main independent variable was HIV infection status. Demographic characteristics (i.e., age, education, marital status, religion, and sexual orientation), behavioral factors (i.e., age at anal sexual debut, years since anal sexual debut, number of men had receptive sex in past year, sexual positioning [insertive only or any receptive], condom use with receptive sex, and any female sexual partners), and concurrent STIs (i.e., rectal gonorrhea, rectal chlamydia, and anal warts) were also evaluated as independent risk factors for HR-HPV. Variables related to immunodeficiency (CD4 counts, viral loads, World Health Organization [WHO] stage, and ART status) were summarized for the HIV-positive MSM. The baseline demographics of HIV-positive and HIV-negative MSM were compared using Pearson χ2 tests for categorical variables and Wilcoxon rank sum tests for continuous variables. Univariate and multivariate Poisson regression models with robust error variance were used to estimate prevalence ratios and 95% confidence intervals (CI) for the association between independent risk factors and anal HR-HPV infection. Size of personal network, as a form of weighting, was included in all multivariate models to account for the RDS design. A directed acyclic graph (DAG) was generated using DAGitty22 to identify the minimal set of a priori confounders (sexual behavior, size of personal network, and age) needed to adjust for the association between HIV infection and HR-HPV without introducing selection bias from over adjustment23 (see Figure, Supplemental Digital Content 2,, for DAG illustration). The final multivariate model adjusted for years since anal sexual debut, sexual positioning, concurrency, and size of personal network. Female partners was not included in the final model because it did not confound the main association (<10% change in estimated effect) and was significantly associated with concurrency. Age was not included in the model because it was positively correlated with years since sexual debut. Analyses were performed using Stata Statistical Software: Release 13 (StataCorp LP, College Station, TX).

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A total of 154 participants (64 HIV-negative and 90 HIV-positive) were included in the analytic sample size, after removing 3 participants with any missing data on a priori confounders (years since sexual debut, sexual positioning, or female partners). Participants missing data on descriptive covariates were retained in the analysis.

Overall, participants were young (median age, 25 years; interquartile range [IQR], 22–28 years; range, 16–38 years) and initiated anal sex at a young age (median age, 16 years; IQR, 13–18 years; range, 7–29 years). Participants engaged in sexual activities both with men (median number of receptive sexual partners, 3; IQR, 1–5) and women (median number of vaginal sexual partners, 1; IQR, 0–2).

Compared with HIV-negative men, HIV-positive men were older, had larger personal networks of MSM, engaged in more unprotected receptive sex, and were diagnosed as having concurrent anal warts (Table 1). For HIV-positive MSM, less than half were receiving ART (n = 39; 43%) at study entry, the median CD4+ cell count was 320 cells/μL (IQR, 221–425 cells/μL), a third (n = 29; 32%) had a viral load greater than 100,000 copies/mL, and 24% (n = 22) had a WHO stage of 2 at enrollment.



The prevalence of any HPV, any HR-HPV, any of the 9 vaccine-preventable HPV strains (6/11/16/18/31/33/45/52/58), and any nonvaccine HR-HPV strain ((35/39/51/56/59/68) was higher in the HIV-positive MSM as compared with the HIV-negative MSM (Fig. 1). Approximately 59% (53/90) of HIV-positive and 83% (53/64) of HIV-negative MSM did not have a prevalent HPV16 or HPV18 infection. HPV35 had the highest point prevalence (34.4%) among HIV-positive MSM, followed by HPV58 (27.8%), HPV51 (26.7%), HPV18 (25.6%), HPV45 (25.6%), and HPV16 (23.3%; see Figure, Supplemental Digital Content 1,, for type-specific prevalence by HIV status). HPV16 had the highest point prevalence (12.5%) among HIV-negative MSM, followed by HPV51 (9.4%), HPV35 (7.8%), HPV58 (7.8%), HPV52 (6.3%), and HPV31 (6.3%; see Figure, Supplemental Digital Content 1,, for type-specific prevalence by HIV status).



As shown in the unadjusted analysis in Table 2, risk factors for HR-HPV included HIV infection, longer duration since anal sexual debut, and larger personal networks of MSM. Younger age and having female sex partners were associated with a lower prevalence of HR-HPV. Initiation of anal sex before age 13 years, any receptive sex in the past year, and increasing numbers of anal receptive sex partners in the past year were positively associated with HR-HPV. For HIV-positive MSM, there was no difference in HR-HPV by category of CD4 counts (<200, 200–349, 350+; P = 0.90), viral load (<100, 100–99,999, 100,000+; P = 0.81), WHO stage (1 vs. 2; P = 0.34), or self-report of ART at study entry (P = 0.94).



As shown in the multivariate analysis in Table 3, HIV infection was significantly associated with a 2-fold increased prevalence of HR-HPV infection (Table 3). The proportion of MSM with anal HR-HPV was approximately 26% higher if they had 10 or more years since sexual debut. Similarly, MSM in concurrent relationships strictly with men had an approximately 32% higher prevalence of anal HR-HPV, as compared with MSM with no concurrent relationships. Practicing any receptive sex was no longer significantly associated with anal HR-HPV.



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Our study of young Nigerian MSM demonstrated a high prevalence of anal HR-HPV during HIV infection. The most prevalent HR-HPV type-specific infections that occurred in both the HIV-positive and HIV-negative MSM were HPV35, HPV58, HPV51, and HPV16, with HPV16 not being the dominant HR-HPV infection among the HIV positive. Given the diversity of HR-HPV infection, most of the HR-HPV types would be prevented with the 9-valent vaccine, except HPV35 and HPV51. Interestingly, a large proportion of our participants were not currently HPV16 or 18 DNA positive, highlighting an opportunity to provide catch-up immunization to prevent infection with the most oncogenic genotypes. In terms of risk factors, HIV infection was the strongest predictor for anal HR-HPV infection. In addition, more than 10 years since anal sexual debut and concurrent relationships with men were independently associated with an increased prevalence of anal HR-HPV infections.

Our baseline prevalence of anal HR-HPV infection in those coinfected with HIV was similar to the prevalence observed in Australia (94%)12 and higher than those reported from North America (ranging from 56% to 80%),7–9 Europe (ranging from 65% to 79%),10,11 Asia (ranging from 58% to 61%),13,14 and the summary prevalence of 74% (95% CI, 64–83) from a meta-analysis.15 Although the Australian study had a similar prevalence, its study population significantly differed in their age composition and sexual risk behavior. The Australian study comprised much older men in their mid-40s with an initiation of sex more than 20 years prior and more than a third reporting more than 500 lifetime number of sex partners. In contrast, our study comprised much younger HIV-positive MSM (79% <30 years of age) with lower risk behavior. Sexual debut occurred 10 years prior, and their personal networks included a median of 35 men. Geographic distributions of HPV prevalence may explain the higher detectability of HR-HPV in our study as compared with the other studies. In a meta-analysis comparing the prevalence of cervical HPV among women with normal cytological findings, the prevalence of HPV was higher in Western Africa which includes Nigeria (19.6%) as compared with North America (4.7%).24 The higher prevalence may also be the result of underreporting of sexual risk behavior because our observed prevalence among the HIV-negative MSM was the same as the prevalence reported from a geographically distinct region (Seattle, Washington). The Seattle study population had a similar age composition and exposure time since sexual debut with another man.25 Other studies of HIV-negative MSM with differing age compositions and exposure times have estimated anal HR-HPV in the range of 27% to 73%.7,9,11–15,26 Additional studies of anal HPV are needed from young MSM in sub-Saharan Africa to confirm the breadth of diversity observed in our study.

Among HIV-positive MSM, HPV35 and HPV51 were among the most common and HPV16 ranked sixth in prevalence. Other studies among Nigerian women documented HPV35 as one of the more prevalent high-risk type-specific infections.27,28 One Nigerian study found that invasive cervical cancers were predominantly associated with HPV16 (68%) and HPV18 (10%) as compared with HPV35 (6%)28; therefore HPV35 and possibly HPV51, although highly prevalent, may not be as persistent or oncogenic as HPV16 and HPV18. Longitudinal studies are needed to better understand persistence of and progression of non-HPV16 or 18 HR-HPVs in Nigeria to better understand their contribution to anal cancer risk.

Similar to other studies, HIV infection and markers of sexual behavior (i.e., longer duration since sexual debut) were independent predictors of anal HR-HPV.7,8,11,12,25,26 The prevalence of anal HR-HPV was higher among MSM who had concurrent relationships with men. Having female partners was initially protective in the univariate analysis. This finding is consistent with a study from China, where female partnerships were not associated with anal HR-HPV.29 Female partners are potentially a surrogate marker of lower exposure to HPV from receptive sex. However, this risk is not mitigated for their female partners given the high prevalence of HIV and HR-HPV among the MSM. Additional studies are needed to find effective interventions that increase uptake of cervical cancer screening among female partners of MSM, who may not be aware of their exposure risk. Other markers of sexual behavior, such as number of receptive partners and unprotected receptive sex, were positively associated with anal HR-HPV.

Our study had a few limitations. Data on lifetime number of sexual partners, one of the strongest sexual risk factors, were not collected in this cohort, but estimates of personal networks of MSM were available and potentially accounted for this risk factor in the analysis. Another strong risk factor for HPV is smoking, which was not collected in our cohort. If smoking behavior is differential by HIV status, then the independent estimates of HIV would move toward the null. Next, participants were asked to report their sexual behavior over the past 12 months, potentially introducing recall bias in terms of their behavior with men, women, and condom use. However, most of these variables were in the expected direction and the precision of these associations would have been strengthened with a larger sample size. Lastly, this was a cross-sectional study that was not able to assess directionality between HIV and anal HR-HPV infections. Despite these limitations, estimates of anal HR-HPV prevalence in Nigeria are not based on a convenient sample and may be generalizable to other young MSM with similar risk behaviors, given that this sample achieved greater than 8 waves of recruitment. There was no significant difference in the prevalence of anal HR-HPV between waves 1–5 and waves 6–10 (data not shown), suggesting that equilibrium was reached.30 Because the sampling design was accounted for in the analysis by adjusting for personal network size, inferences about the study population are generalizable to other comparable MSM populations in sub-Saharan Africa. Overall, these baseline estimates of anal HR-HPV are needed to inform follow-up analyses on incident and persistent infections.

In summary, our study documents a high burden of anal HR-HPV infection among young MSM from Nigeria, particularly those infected with HIV. HPV35, HPV58, and HPV51 were more common than HPV18, HPV45, and HPV16 among the HIV-positive MSM. The high proportion of MSM naïve to HPV16 and HPV18 offers an opportunity to provide catch-up immunization to prevent anal cancer. Future studies are needed to assess anal HR-HPV persistence and progression to neoplasia given the breadth of types detected in this study to better understand the potential effectiveness of the 9-valent vaccine to reduce the burden of HPV-associated malignancies.

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