Adult male same-sex behaviour is criminalized in Kenya, as in many other countries in Africa, and is highly stigmatized in African society. Front-line health workers are often ill prepared to provide care and appropriate risk-reduction counselling to MSM . Despite the prevailing belief among researchers in the recent past that anal intercourse between men was not epidemiologically significant to the African HIV-1 epidemic , a growing body of evidence documents populations of MSM with high HIV-1 prevalence in many African countries [3–6].
A recent systematic review of 57 HIV-1 incidence studies in sub-Saharan Africa over the period 1987–2008 identified no cohort studies involving MSM participants or including anal sex as a risk factor for HIV-1 acquisition . The highest reported HIV-1 incidence rates in Africa occurred in the 1990s among urban female sex workers, with over 16 infections per 100 person-years of follow-up . Young people, individuals in concurrent or multiple partnerships, and individuals with a current or recent sexually transmitted infection (STI) were consistently identified as being at risk for HIV-1 infection. A recent global review of HIV-1 incidence estimates in MSM over the period 1995–2010 identified studies from 15 countries only, including two reports from Asia, and a preliminary report from Africa (present study) . Price et al.  reported in 2012 an HIV-1 incidence of 6.8 per 100 person-years for MSM in Kenya over the period 2005–2008, including data from Nairobi and coastal Kenya.
Despite recent advances in the recognition of MSM in Africa, research of HIV-1 risk in this group to date has been based almost exclusively upon HIV-1 prevalence studies  and has not included a distinction between MSM who reported sex with men and women, and MSM who reported sex with men only. Earlier, we reported that the high prevalence of HIV-1 in Kenyan MSM is probably due to unprotected receptive anal intercourse (RAI) . In the present study, we present estimates of HIV-1 incidence, correlates of HIV-1 acquisition among Kenyan MSM during 6 years of follow-up, and viral load measurements in the 2 years following seroconversion.
In July 2005, a prospective study of men and women considered to be at high risk for HIV-1 acquisition was initiated in a research clinic in Mtwapa town, approximately 20 km north of Mombasa. Adults aged 18–49 years were eligible if they met any of the following criteria: HIV-1-negative and reporting any of transactional sex work, a recent STI, multiple sexual partners, sex with an HIV-1-infected partner, or anal sex during the 3 months before enrolment . The initial focus of recruitment was on female sex workers and high-risk heterosexual men. Men who reported anal intercourse with another man in the preceding 3 months became the focus of recruitment in late 2005. In March 2008, a second research clinic in Kilifi town, approximately 40 km north of Mtwapa, started to enrol additional MSM. While MSM could only be engaged for HIV-1 prevention, care and research in the context of providing services to all high-risk men and women, the population for the current study is limited to MSM.
MSM were recruited at two walk-in voluntary counseling and testing centres adjacent to the research clinics . In addition, identification and recruitment of MSM was conducted by a team of 10–15 peer mobilizers, who approached individuals via personal networks and at social venues [9,10]. Recruitment activities encompassed a region of coastal Kenya extending from Malindi in the north (60 km from Kilifi) to Mombasa in the south. Meetings were held with local stakeholders to enlist support for the ongoing research and prevent misunderstanding in the target communities . Written informed consent was obtained from all study participants. The study was approved by the ethical review board at the Kenya Medical Research Institute.
Behavioural assessment and clinical procedures
Detailed procedures are described elsewhere [12,13]. Briefly, enrolment and follow-up assessments included face-to-face interviews using standardized questionnaires to ascertain recent behaviour and genitourinary symptoms ; HIV-1 testing; and a physical examination, including genital examination . Urethral swabs were collected if urethral symptoms were reported or urethral discharge was clinically apparent. Proctoscopy and rectal screens were offered to men who reported recent RAI and who also had anorectal pain, rectal discharge, or bleeding. Persons who tested HIV-1-seronegative at initial screening were enrolled and attended either monthly (when RAI was reported) or quarterly behavioural, clinical, and laboratory follow-up visits using the same procedures. Those who had at least one follow-up sample available for testing through April 2011 were analysed in this study. Participants were considered lost to follow-up when they had not reported to the clinic for a period of 6 months since their last study visit.
Treatment of minor illnesses and risk-reduction counselling
At all visits, risk-reduction counselling, condoms, and water-based lubricants were provided. Participants with genital symptoms were provided syndromic treatment, and laboratory-diagnosed infections were treated following Kenyan Ministry of Health guidelines. After July 2010, standard treatment for gonorrhoea was changed from norfloxacin to cefixime, due to evidence of increasing resistance of Neisseria gonorrhoeae to fluoroquinolones .
Screening for sexually transmitted infections
HIV-1 testing was performed using two rapid test kits (Determine; Abbott Laboratories, Abbott Park, Illinois, USA; Unigold; Trinity Biotech plc, Bray, Ireland) in parallel. Discordant rapid HIV-1 test results were resolved using an ELISA test (Genetic System HIV-1/2 plus O EIA; Bio-Rad Laboratories, Redmond, Washington, USA). All HIV-1-negative samples were tested for p24 antigen (Vironostika HIV-1 p24 ELISA; Biomérieux Ltd, Marcy L’Etoile, France), and pre and post seroconversion plasma samples were tested for HIV-1 RNA level (Amplicor Monitor vs. 1.5; Roche, Basel, Switzerland), with a positive result defined as more than 400 copies/ml.
The estimated date of HIV-1 infection (EDI) was calculated as follows : 10 days before the sample collection date when the sample had a positive HIV-1 RNA level and negative p24 antigen and HIV-1 serology; 14 days before a positive p24 antigen test (with or without a positive HIV-1 RNA level); or the mid-point between a previously negative and subsequently positive HIV-1 serologic test, in the absence of either a positive HIV-1 RNA level or p24 antigen test. When volunteers had a positive p24 antigen test, or documented HIV-1 seroconversion, they were invited to enrol in an acute HIV-1 infection study with frequent blood sample collection for HIV-1 plasma viral load (PVL) and CD4 T-cell assessments in the first 3 months following EDI and quarterly collections from 3 months up to 2 years after EDI.
Gonococcal infection was defined as the detection of Gram-negative, intracellular diplococci consistent with N. gonorrhoeae in urethral or rectal secretions , and recent gonorrhoea as urethral or rectal gonococcal infection within a 6-month window .
Prevalent syphilis infection was diagnosed by a positive rapid plasma reagin (RPR) titre confirmed by Treponema pallidum haemagglutination assay (TPHA). Incident syphilis was defined as a four-fold increase in RPR titre confirmed by TPHA. Serological testing for herpes simplex virus 2 (HSV-2) was performed on archived samples (HerpeSelect-2; Focus Diagnostics, Cypress, California, USA) as described elsewhere . Briefly, all participants had their enrolment plasma sample screened for HSV-2 antibodies. Volunteers who had a negative HSV-2 serology at enrolment had their last follow-up sample tested to define HSV-2 serostatus at the end of the study. For participants who were HSV-2-seropositive at their last visit, intervening samples were tested to determine seroconversion timing. For those participants who seroconverted for both HSV-2 and HIV-1, timing of HSV-2 seroconversion was confirmed using western blot testing . HSV-2 serostatus for each participant was defined as seronegative, prevalent at enrolment, or incident during follow-up.
Data management and analysis
Questionnaire, clinical, and laboratory data were entered into a secure database. Individual and aggregate data were subjected to routine accuracy checks by research staff and periodic review by study monitors. Data cleaning, recoding, and analysis were conducted using Stata version 11 (StataCorp, College Station, Texas, USA).
Sociodemographic data were collected at enrolment. At each visit, men were asked to report whether they had been sexually active with men, women, or both. As in our previous work , this variable was aggregated across all study visits and used to classify MSM into two risk groups for analysis: men reporting sex with men exclusively (MSME), and men reporting sex with both men and women (MSMW). Reported sexual intercourse and condom use in the week before each visit were used to define three outcomes: ‘abstinent’ in which sexual activity was not reported, ‘100% condom use’ in which sexual activity occurred and condoms were used for all reported sex acts (defined as either vaginal or anal intercourse), and ‘unprotected’ in which sexual activity occurred but condoms were not used for all sex acts . Other time-dependent sexual risk behaviour variables recorded at each visit included receipt of payment for sex, payment for sex, participation in group sex (defined as sex with more than one person at the same time), anal intercourse (whether receptive or insertive), and rape. Oral sex was not assessed. Nonsexual behaviour variables included use of alcohol (in month prior to visit) and use of intravenous drugs since the last visit. Iatrogenic exposure to HIV-1 was based on any medical injection or blood transfusion since the last visit.
Two seroconverters had no behavioural and clinical data collected in the 3-month period prior to seroconversion and were excluded from analysis for lack of precision. Associations between categorical variables were tested using Pearson's χ 2 or Fisher's exact tests as appropriate. Associations between nonnormally distributed continuous and categorical variables were assessed using the Wilcoxon rank-sum test or Spearman's rank correlation. Reported P values are two-sided.
HIV-1 incidence rates were expressed as incidence per 100 person-years. Incidence rates for risk groups were compared by log-rank test. We evaluated potential risk factors for HIV-1 incidence as either fixed covariates (e.g. circumcision status) or time-varying covariates (e.g. transactional sex in previous 3 months). Incidence rate ratios (IRRs) were used to describe associations between covariates and estimated HIV-1 incidence. A population-averaged multivariable Poisson model with robust variance estimates was used to estimate adjusted incidence rate ratios (aIRRs). Factors identified a priori (e.g. age) and factors associated with prevalent or incident HIV-1 with P value 0.1 or less were included in the initial multivariable model. To reduce the number of predictors, only those factors significant at P less than 0.10 in the initial multivariable model were retained in the final multivariable model.
Between July 2005 and April 2011, 449 HIV-1-negative MSM contributed at least one follow-up visit (Table 1). Of these, 372 (82.9%) were MSMW and 77 (17.2%) MSME. Baseline sociodemographic characteristics differed by age (a larger proportion of MSME were between 18 and 24 years), marital status (only two MSME were currently married), and personal assets; MSME reported possession of a greater number of material assets than MSMW.
Sexual risk behaviour and sexually transmitted infection prevalence at enrolment
Participants reported a median of two sex partners [interquartile range (IQR): 1–3] and three sex acts (IQR: 1–6) in the last week; 23.6% of sex acts were protected (Table 1). This was similar between MSMW and MSME. Group sex was commonly reported by both MSMW and MSME, rape and intravenous drug use were rare, and the majority of men used alcohol. As our data revealed previously, MSMW reported more often insertive anal intercourse (IAI), and MSME more often RAI. Over two-thirds of participants reported being paid for sex (no difference between MSMW and MSME), whereas over a third paid for sex themselves (38.7% of MSMW vs. 13.0% of MSME, P < 0.001). Recent urethral and rectal gonorrhoea was diagnosed in 2.0 and 0.4% of all men, respectively. Prevalence of genital sores was 11.1%; syphilis 1.6%; and HSV-2 seropositivity 18.7%.
HIV-1 incidence estimates and correlates of infection
The 449 participants contributed 743.9 person-years, with median follow-up times of 21.0 months (IQR: 8.6–37.4) for MSMW and 4.6 months (IQR: 2.5–16.5, P < 0.001) for MSME. Sixty-four men acquired HIV-1 during follow-up, for an estimated HIV-1 incidence of 8.6 [95% confidence interval (CI) 6.7–11.0] per 100 person-years (Table 2). HIV-1 incidence was 5.8 (95% CI 4.2–7.9) per 100 person-years among MSMW and 35.2 (95% CI 23.8–52.1) per 100 person-years among MSME (P < 0.001, Fig. 1). Loss to follow-up was 25.7 (95% CI 22.3–29.6) per 100 person-years; 23.9 (95% CI 20.5–27.9) per 100 person-years among MSMW and 42.2 (29.5–60.4) per 100 person-years among MSME (log-rank test, P = 0.009). In univariate analysis, HIV-1 acquisition was associated at P of 0.10 or less with reporting exclusive sex with men, younger age, being single, having unprotected sex, having been paid for sex, not having paid for sex, IAI, RAI, group sex, having been raped, genital sores and a recent laboratory-diagnosed gonorrhoea infection (details in Table 2). In multivariable analysis, exclusive sex with men (aIRR 3.7, 95% CI 2.1–6.5), recent unprotected sex (aIRR 2.1, 95% CI 1.1–4.1], relative to no recent sexual activity), RAI (aIRR 9.7, 95% CI 3.8–25.1), group sex (aIRR 1.9, 95% CI 1.0–3.4), and gonorrhoea infection in the past 6 months (aIRR 14.7, 95% CI 8.3–26.0) were strongly associated with HIV-1 acquisition, after adjustment for age, marital status, transactional sex, IAI, having been raped, and genital sores.
Herpes simplex virus 2 acquisition
Of the 64 men who seroconverted for HIV-1, 45 (70%) were HSV-2-seronegative throughout the observation period, 16 (25%) were HSV-2-seropositive at enrolment, and three (5%) had a change of HSV-2 antibody status consistent with HSV-2 seroconversion. Of these three men, two had an incident HSV-2 infection approximately 5 months before, and one just before or at HIV-1 acquisition. Thirty-seven men seroconverted for HSV-2 in the absence of HIV-1 acquisition.
A total of 42 men acquired a urethral or rectal gonorrhoea infection during follow-up. The estimated incidence of gonococcal infection was 5.9 (95% CI 4.4–8.0) per 100 person-years overall. Incidence was 5.6 (95% CI 3.9–8.3) per 100 person-years for MSMW and 9.3 (95% CI 4.2–20.7) per 100 person-years for MSME (P = 0.6). Incident gonoccocal infections occurred in the 6 months prior to HIV-1 acquisition in six men, including one that coincided with the timing of HIV-1 acquisition. The median time from the incident gonorrhoea infection to HIV-1 acquisition in these six men was 57 days (IQR 22–128).
Postinfection viral dynamics
HIV-1 RNA dynamics were assessed in 63 seroconverters. In the first 2 years (104 weeks) after infection, 517 PVL measurements were obtained. PVL was more than 4 log10 copies/ml at 230 (73.4%) of 313 visits in MSMW and 153 (75.0%) of 204 visits in MSME (Fig. 2a). At corresponding time-points for which CD4 T-cell count measurements were available (n = 504), CD4 T-cell counts were less than 350 cells/μl, the current threshold for antiretroviral therapy (ART) initiation in Kenya, at only 66 visits (13.1%; Fig. 2b).
We documented very high HIV-1 incidences among a large group of MSM in Coastal Kenya. Among MSME, over one third acquired HIV-1 within 1 year of study enrolment, whereas HIV-1 incidence in MSMW (82.9% of our cohort) was 5.8 per 100 person-years. These rates are among the highest currently documented in Africa [6,7]. Previous research in this cohort has demonstrated that many MSM have concurrent sexual partnerships . Most sex partners of MSM in this cohort were Kenyan [12,20], and HIV-1 isolates from a subgroup of MSM in this cohort were similar to isolates from the general population in Kenya . Among MSM who seroconverted during follow-up, PVL remained high (>4 log10 copies/ml) in the 2-year period following infection. Because CD4 T-cell counts in these seroconverters remained above the threshold for ART initiation in Kenya, these men posed a significant risk of HIV-1 transmission to their sexual partners during the study period.
The very high HIV-1 incidence among MSM from Coastal Kenya may be the result of studying an interconnected network of adults with ongoing high-risk sexual activity. Interestingly, the estimated HIV-1 incidence in MSM who participated in a study in Nairobi during 2007–2008 was similar (9.1 per 100 person-years) to our estimate among Coastal MSM (8.6 per 100 person-years) . Given that up to 40% of new HIV-1 infections are likely transmitted by individuals in the early phase of HIV-1 infection (within 6 months following the estimated date of infection) , interventions aiming to reduce HIV-1 acquisition and transmission among MSM in Kenya should include frequent, targeted HIV testing and linkage to care, with a strong focus on effective biomedical interventions such as preexposure prophylaxis (PrEP) and early ART . Such interventions will benefit both MSM and the wider, primarily heterosexual population who are connected to Kenyan MSM through their sexual networks.
We identified several risk factors that were independently associated with HIV-1 acquisition in this population. Men who reported unprotected sex or group sex had a two-fold higher risk, exclusive sex with men had a four-fold higher risk, RAI had a 10-fold higher risk, and those who had a laboratory-diagnosed gonorrhoea infection in the past 6 months had a 15-fold higher risk, respectively, of acquiring HIV-1 when compared to men who did not report these risk factors, after adjustment for potentially confounding factors. The risk estimate of RAI is similar to those from previous reports comparing the risks of RAI to those of penile-vaginal intercourse [24,25]. MSME reported significantly less IAI and more RAI than MSMW at study enrolment. MSME in our cohort were younger, better off financially than MSMW, and extremely vulnerable to acquiring HIV-1. These MSME, who have also been referred to as ‘queens’ in Kenya , experience very strong societal rejection and may face greater barriers than MSMW to accessing medical services, including ART. Such barriers may impair their ability to attain virologic suppression, relative to MSMW.
Unprotected sex derived from a composite variable based on the number of sex partners, number of sex acts, and number of sex acts protected by a condom in the week prior to the assessment. Targeting any of these components for behaviour change intervention is important in itself, but may not be a sufficient strategy for reducing HIV transmission among MSM [26,27]. Very few studies have found group sex to be practised in African settings [28,29], and our study is the first to document that group sex is an independent risk factor for HIV-1 acquisition in African MSM. Anecdotally, participants who reported group sex said that unprotected sex is common during these encounters, which frequently happens when alcohol is taken in excess. Our data did not assess characteristics of group sex or situations in which group sex commonly occur. That one of six men reported it at study enrolment suggests that this practice is relatively common. Risk-reduction counselling targeting MSM needs to explore whether men participate in group sex and provide counselling about the high risk of HIV-1 and STI acquisition and transmission due to these encounters.
Gonorrhoea incidence was 5.6 per 100 person-years in MSMW and 9.3 per 100 person-years in MSME based on detection of Gram-negative, intracellular organisms compatible with N. gonorrhoeae in Gram-stained urethral or rectal secretions collected from symptomatic men. Our estimated incidence is likely to be an underestimate as the microscopic method used for detection is relatively insensitive . We have recently reported a relatively high prevalence of asymptomatic infections and of quinolone-resistant gonorrhoea in this population [14,30]. Persisting inflammation of urethra or rectum due to unsuccessfully treated or undetected infections may have contributed to the increased risk for HIV-1 acquisition we observed . Of note, the World Health Organization's new guidelines for STI management in MSM and transgender people recommend that asymptomatic MSM who report RAI in the past 6 months and have multiple partners or a partner with a STI should receive treatment for gonorrhoea and chlamydia . Most MSM in this study would have been eligible to receive presumptive treatment for gonorrhoea and chlamydia infection at cohort enrolment per the new WHO recommendation. A recent study conducted in our MSM cohort revealed that for every seven MSM meeting WHO criteria for presumptive treatment, one asymptomatic anorectal infection (detected by nucleic acid amplification test screening) would have been treated .
In the ‘EXPLORE’ study involving almost 4300 HIV-1-seronegative MSM with an HSV-2 prevalence of 20.3% and HSV-2 incidence of 1.9 (95% CI 1.6–2.2) per 100 person-years, both incident and prevalent HSV-2-infections increased the risk of HIV-1 acquisition . HIV-1 acquisition has been strongly associated with incident HSV-2 infection among heterosexual African men , and with self-reported genital ulcer disease in a recent analysis of over 300 Kenyan MSM (a subset of the present study) . We have previously reported that HIV-1 acquisition was associated with HSV-2 acquisition in this population . However, prevalent HSV-2 was not a risk factor for HIV-1 acquisition in this study, and only three of 64 incident HSV-2 infections occurred before or around the time of HIV-1 acquisition. Because women in the same population have a much higher prevalence of HSV-2 (50.8 vs. 20.0% in men) , it is possible that men in our study population acquired HSV-2 infection primarily from female partners and HIV-1 infection primarily from male partners, through unprotected RAI.
This study has a number of limitations. First, MSM populations have been mobilized through peer educators who frequently reported sex work. As such, MSM enrolled in this study likely do not represent the wider and largely hidden nonsex worker MSM population in Coastal Kenya. Second, our data were collected through face-to-face interview, which may be less sensitive than other methods such as audio computer-assisted self-interview (ACASI) for reporting sensitive information . Third, STI screening was targeted at symptomatic individuals and employed a relatively insensitive methodology due to budget constraints. Finally, as this is the first ongoing longitudinal study of MSM in Kenya, men's willingness to participate was likely impacted by the need for MSM participants to protect their safety and privacy, especially as the most vulnerable men, MSME, had the highest loss to follow-up. Notwithstanding these limitations, our study demonstrates that MSM can be engaged to participate in longitudinal research in Kenya.
In summary, whereas cross-sectional studies involving MSM in Africa have shown very high HIV-1 prevalence among MSME relative to MSMW [6,9,35], this is the first study that has estimated HIV-1 acquisition risks among MSMW and MSME together. Our findings suggest that unprotected sex, RAI, exclusive sex with men, group sex, and coinfection with gonorrhoea are the primary biological drivers of the HIV-1 epidemic among MSM from coastal Kenya. Although some risk factors are potentially modifiable and require both structural and targeted behaviour and public health interventions, the very high HIV-1 incidence and sustained high viral loads in the majority of MSMW and MSME for up to 2 years following seroconversion highlight the urgent need for both PrEP and early ART interventions in this population.
The authors would like to thank the International AIDS Vaccine Initiative (IAVI) for supporting the high-risk cohort studies in Kilifi, and staff in the HIV/STI project at the Kenya Medical Research Institute in Kilifi for their commitment to serving MSM. They are also grateful for support and guidance provided by the KEMRI-Wellcome Trust Research Programme to carry out research with stigmatized and vulnerable populations. They thank James Tang and Wei Song, at the University of Alabama for their kind assistance of the analysis of RNA viral load and CD4+T cell dynamics in 63 seroconverters, and Larry Corey, Rhoda Morrow, and Anne Cent, for kindly testing their seroconverter samples by herpes simplex virus 2 (HSV-2) western blot. HSV-2 testing received support from the University of Washington Center for AIDS Research (CFAR), an NIH funded program (P30 AI027757). They are grateful for comments by two anonymous AIDS’ reviewers on an earlier version of this article. This work was made possible in part by the generous support of the American people through the United States Agency for International Development (USAID). The contents are the responsibility of the study authors and do not necessarily reflect the views of USAID, the NIH, or the United States Government. This report was published with permission from KEMRI.
E.S. designed the HIV-1 incidence cohort study, performed data analysis, and wrote the first draft of the article.
H.S.O. performed data acquisition and the full data analysis.
A.S. performed initial data analysis and article editing.
M.M. performed behaviour and clinical data collections.
E.W. performed data acquisition and quality assurance.
G.F. assisted with and advised on data analysis, and article editing.
N.P. and E.M.van der E. supported engagement of local stakeholders.
M.A.P. and R.S.M. designed the HIV-1 incidence cohort study and did article editing.
S.M.G. designed the HIV-1 incidence cohort study, and did data analysis and critical revision of the article.
Conflicts of interest
The authors declare that they have no conflicts of interest.
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