With additional reporting by Lance Sherriff
The HIV prevalence among men who have sex with men (MSM) in South Africa is much higher than among men in the general population according to three separate epidemiological surveys presented at the South African AIDS Conference earlier this month. 43.6% of the participant’s in one study in Johannesburg and Durban (eThekwini) were HIV-positive; in another, the prevalence among men between the ages of 20 to 24 who identified themselves as gay was 49%. Most of these surveys’ participants were black — and the one study that could look somewhat at race (in Cape Town) found a significantly higher prevalence of HIV among participants from traditionally black townships than among those from coloured townships.
But even though the HIV prevalence varied somewhat from study to study (depending upon the sampling method, race of the participants and study site), they each found a heavy burden of HIV among young MSM — especially those who are gay-identified — to which the public health system has not been responding appropriately.
“There are actually parallel HIV epidemics in South Africa,” said Professor Laetitia Rispel of Wits University, who was one of the principal investigators of the Johannesburg/eThekwini’s Men’s Study (JEMs). “There’s the generalised heterosexual epidemic but there’s also a hidden, perhaps forgotten epidemic, among MSM, who to a large extent have fallen off the agenda over the last 15 years.”
“Whilst HIV infection amongst MSM was the focus in the early phases of the epidemic in South Africa, there is currently very little known about the epidemic amongst MSM in the country,” said the National Strategic Plan on HIV and AIDS 2007-2001.
In South Africa in the early 1990s, just like most of the industrialised world, HIV was associated with the visible gay male population, who, it was widely thought, were mostly white. The country was in denial about at least two things: 1) that HIV wasn’t a problem in the general population, and 2) that men of all races were having sex with men. The reality of the epidemic among the general population proved too much to disguise, but as in much of the rest of Africa, MSM continue to be a marginalised, hard to reach and under studied population.
However, in most of the developing world, the studies that have been conducted indicate that MSM are at a higher risk of HIV infection than the general population. According to a review in PLoS Medicine, the prevalence among MSM is about ninefold higher than the general population in medium-high HIV prevalence countries, though only a couple of sub-Saharan African countries were included.1 In the last couple of years, this understanding has become more nuanced as data have become available for many other African countries (see accompanying article).
In South Africa, by 2007, the NSP finally called for more information on HIV among MSM and also for programmes to reach the most at risk populations, including MSM. There were so little reliable data that the country was unable to report on indicators for MSM for the UN General Assembly progress report on universal access to HIV treatment and prevention submitted to the UN early 2008. Since that time, several studies have been launched.
The JEMS study
The JEMS study was a collaborative effort between the Wits University in Johannesburg, the Human Sciences Research Council (HSRC) and the Medical Research Council.2 Before the survey, the researchers conducted extensive background research with a literature review, focus group discussions and interviews with key ‘informants’ from the LGBT community in Johannesburg, Durban, Cape Town, Pretoria and Pietermaritzburg. The survey of HIV prevalence and behaviour was focused on Johannesburg and Durban, because other groups were conducting similar surveys in Cape Town and Pretoria.
The survey recruited men using respondent-driven sampling (RDS) — a form of chain sampling which has been used extensively in other studies to recruit members of “hard to reach” populations. Eligibility requirements for the study included being male, aged 18 years or more, and having had sex with at least one other male in the past 12 months, and living, working or socializing in Johannesburg or Durban. With RDS, the initial participants are called “seeds” and these were deliberately chosen to be diverse in terms of age, race, socio-economic status, and to have large social networks. Each participant was asked to recruit up to three more participants. They were reimbursed for their participation, with a R40 (£3) cash and R40 voucher and were also reimbursed R40 for each additional participant they recruited (max. R120) (these amounts were thought to be enough of an incentive without being coercive).
After answering the survey questionnaire, 95% of the subjects provided dried blood spot samples that were linked to his answers and sent to the laboratory anonymously. Participants were also offered free VCT using a rapid HIV test with same-day results as an additional optional service to participants.
The study accrued 285 participants in all (204 JHB and 81 Durban). 88% were black African (in a separate poster presentation, the researchers noted that despite their efforts and use of RDS, the population wasn’t as diverse as they would have liked, with very few white men for instance).3
Most of the participants were young — ages ranged from 18 to 61 years old — but two-thirds were under 25 years old (mean age 24.5 years; median age 22 years). 78% self-identified as homosexual or gay; 19% bisexual; 2% heterosexual or straight and 2% as (which included transgender individuals. 54% had greater than or equal to a grade 12 education.
In the 266 who tested, the unadjusted HIV prevalence was 43.6% among the participants. However, the researchers made some adjustments for the RDS-method to take into account that people tend to recruit people similar to themselves (and with similar HIV status), and came up with a prevalence of 38.3% that should be more representative for the MSM in this setting.
This prevalence was “at least twice as high as what one would expect from the general population,” said Dr Carol Metcalf, one of JEM’s investigators. In the national household survey conducted in 2005, the HIV prevalence among men aged 30 to 49 was 11.7%; and the ASSA (Actuarial Society of South Africa) estimate for 2008 of men aged 30 to 49 was 15.9%.4
In general, high-risk sexual behaviour was more common among people who were HIV-positive than those who were HIV-negative. In the previous 12 months, almost one in two participants — around 46% — reported having unprotected anal intercourse within the past year. The HIV-positive participants were more than twice as likely to have receptive unprotected anal intercourse within the past year. HIV-negative men reported an average of five partners in the past year while HIV-positive men reported an average of 7.5.
The participants reported that condoms were often unavailable and condom accidents were common. 55% of the respondents reported that they didn’t have a condom available when they needed one. 42% reported at least one instance of condom slippage and 58% reported an instance of condom breakage in the past year. In addition, many participants reported using lubricants that actually reduced the protective effect of condoms, such as Vaseline or lotion (which are more readily available in South Africa and much less expensive that the water-based lubricants).
Seventy three per cent of the participants reported that they had sex under the influence of alcohol in the past year (and there was no difference between HIV-negative or HIV-positive participants). Another interesting finding was that more than a third of participants reported having experienced sexual coercion — which was significantly associated with being HIV-positive.5
Of note, the men in the sample generally perceived their risk to be low. Prof Rispel said that one reason for this, which came out of focus group discussions, was that most thought that heterosexuals in South Africa were at greater risk of getting HIV than MSM. 57% of the participants reported that they knew their HIV status, but only two-thirds of those who knew their status had disclosed it to a sexual partner within the past year.
Dr Metcalf noted that the survey also included some questions about sex with women. “What is striking from these findings is that the vast majority of HIV-positive men in our study (reported) that they have never had sex with a women,” she said. Only 36 reported ever having had sex with women, and only one out of five of the HIV-positive participants. In the last year very few had had sex with women, and even fewer had unprotected or regular sex. Since there was such a low degree of sexual interaction with women, the JEMS team concluded that the epidemic of HIV among MSM probably does not overlap much with the larger HIV epidemic in South Africa; it is rather running in parallel.
However, Dr Metcalf stressed that this cohort may not be absolutely representative of MSM in South Africa:
“Our participants were predominantly young, gay, black Africans who do not think they were ‘representative of MSM in general or even MSM in the two cities. They don’t actually know what a representative sample would look like,” she said.
But it isn’t clear that the other samples described at the South African AIDS conference were entirely representative either.
A survey in Soweto
One was another RDS survey, conducted in South Africa’s largest township, Soweto, which comprises 85% of the Metro Johannesburg population. This survey seemed to draw in a cohort with somewhat different characteristics, with a much higher proportion of men who categorise themselves as bisexual or straight.
According to Sibongile Dladla, of the Perinatal HIV Research Unit (PHRU) in Johannesburg, MSM in Soweto are “stigmatised and hidden” and unlike other settings in the country, there were no data from LGBT community-based organisations providing HIV services to this population. So researchers from PHRU set up the Soweto Men’s Study to better characterise the MSM population in the township, estimate the HIV prevalence; and determine the social behavioural predictors of HIV infection.6
The study included men over 18 years of age who had had oral or anal sex with another man in the last six months and who lived, worked or socialized in Soweto. Again, “seed” participants were used to recruit their peers over a period of 30 weeks, and were compensated with coupons (R30 or US $5 gift cards, limited to 3 to 5 per participant). Recruitment continued until the target sample size was achieved. Participants were administered a questionnaire, and then offered VCT.
Soweto Men’s Study results
378 men were recruited, aged between 18 and 58 years old (median=23). 99.9% were black South African residents of Soweto (40% Zulu, 17% Sotho, 12% Tswana). Ms Dladla stressed that unemployment is high in Soweto, with 77.5% of the participants earning less than R500 per month. Of note, 33.6% of those in the cohort were circumcised.
About 81% agreed to be HIV tested for the survey though many declined their results (including 29% of new HIV-positive diagnoses). About one out of five of those who tested positive already knew their status. Fifteen per cent had never tested prior to the study; 59% had not tested within the last year.
Twenty per cent of those who consented to VCT, tested HIV positive, but an adjustment for the RDS method suggested the representative prevalence for this population would only be 10.9% (95% Confidence Interval (CI) 6.5-14.6). However, as noted earlier, this sample seemed to have markedly different sexual identities and behaviour from the JEMS cohort.
Only 34.1% identified themselves as gay. 30.4% claimed to be bisexual, and another 31.7% said they were straight. 51.2% claimed to have a regular female partner, with 48.7% reporting at least one female partner among their last five partners. 37.8% reported having unprotected sex with women. Of note, adjustments for the RDS pushed the likelihood of heterosexual behaviour higher. In fact, one has to question whether a significant proportion of the sample may have actually been completely straight.
Seventy three per cent reported having a regular male partner. And yet, in marked contrast to the previous cohort, only 28.6% reported unprotected insertive anal intercourse in the last 6 months, and only 17.5% had unprotected receptive anal intercourse in the previous 6 months.
HIV prevalence among the gay-identified individuals was markedly higher: 47% of those tested overall, 34.5% after adjustment, while the prevalence among ‘bisexual or straight’ was 13.6%, or 9.4 after adjustment.7
An analysis by age and sexual identity was also telling. In South Africa, 3.3% of young men aged 15-19, and 6% of men aged 20-24 are HIV-positive. This compares to 9.4% and 23.9% of women in the same age groups. In this study, the rate for all the participants overall was 8.5% and 38.5% for the same age groups; but among the gay-identified participants, 9.8%, and 49% respectively were HIV-infected.
“The epidemic appears to be spreading rapidly among young, gay-identified MSM,” said Ms Dladla.
Soweto MSM risk factors for HIV
OR (95% CI)
Age > 25
3.8 (3.2 - 4.6)
2.3 (1.8 - 3.0)
Income < R500
1.4 (1.2 - 1.7)
3 to 5 partners in the past 6 months
1.9 (1.4 - 2.6)
Buy drugs / alcohol for male partner
3.9 (3.2 - 4.7)
4.4 (3.5 - 5.7)
Regular female partner
0.2 (0.2 - 0.3)
0.2 (0.1 - 0.2)
A comparison of townships in Cape Town
However, a study in Cape Town, which did not use RDS, also found a higher rate of bisexuality and female partners among black MSM. But the black MSM in this study were three times more likely to be HIV-positive as coloured MSM, who were more likely to be exclusively gay-identified.
“To date, there has been no assessment of whether sexual risk behaviours and HIV prevalence among men who have sex with men (MSM) vary between historically distinct black and coloured townships in Cape Town,” said Earl Ryan Burrell of the Desmond Tutu HIV Foundation (DTHF).
So in partnership with Johns Hopkins University, Burrell and colleagues at DTHF conducted an anonymous, venue-based HIV-risk behaviour and prevalence assessment of 200 self-identified MSM from townships (some traditionally black, others traditionally coloured) in Cape Town, South Africa. Over a period of 27 days, health workers administered a demographics and sexual risk behaviour questionnaire and an oral HIV test at twelve venues know to be frequented by MSM.8
Researchers soon noticed a difference in HIV prevalence associated with data collected at separate venues — which depended on whether they were in traditionally black versus coloured townships (which the researchers used as a proxy for race).
Cape Town r esults
In Cape Town 25.5% (51/200) of the cohort were HIV positive, with a significantly higher prevalence of 37.3% (38/102) among black MSM compared to 12.5% (11/88) among the coloured MSM (p=0.000). (Ten individuals were mixed race and excluded from this analysis).9
With such a profound difference in HIV prevalence between the two populations, the researchers looked at whether any demographic or behavioural characteristics would explain differences in risk.
There were no significant differences between MSM in traditionally black versus coloured townships in age (mean 25.9 years, range 18-49) or high school education, with 10.5% (20/190) having had less than a matric education. Only 1.4% of the sample subjects identified themselves as either straight or heterosexual. The mean number of male sexual partners in the previous six months was 4.2; about 22.1% (32/145) of the sample reported inconsistent condom use with casual partners; 25.3% (48/190) reported ever receiving treatment for an sexually transmitted infection; while 19.5% reported engaging in transactional sex.
There were some significant differences however, such as a higher rate of unemployment in the black township. There were also differences in sexual identity. Transgender MSM were much more common in the coloured townships. About 25.0% of black MSM identified as bisexual compared to 12.5% of coloured MSM (p=0.035), and black MSM had a mean of 0.8 female partners in the previous 6 months compared to 0.1 female partners among coloured MSM (p=0.0016). As far as sexual behaviour went, coloured MSM were less likely to use condoms with their main male partner than black MSM; black MSM were less likely to have tested for HIV in the last six months, and more likely to report using petroleum-based lubricants with condoms.
However, only a number of variables were significant predictors of HIV infection in univariate analysis: being sampled in a black township (p=0.000), having less than a matric education (p=0.009), reporting current unemployment (p=0.007), and not having had an HIV test in the previous 6 months (p=0.002) (each of these also remained significant in the multivariate analysis). But no sexual risk criteria were significantly associated with HIV positivity in this sample.
Nevertheless, Burrell suggested that “the variation in HIV prevalence here may be driven by the community-specific background HIV infection.” In other words, it is theoretically possible that HIV risk in the background general population could provide a baseline prevalence, which is then amplified within the respective MSM population.
Burrell noted that it would take further data looking at HIV clades, and utilizing phylogenetic tree and molecular clock analysis to determine if HIV epidemics among MSM in Cape Town are parallel or linked to a more generalized epidemic. Indeed, years ago, data suggested that most of the HIV among MSM in this population was HIV-1B, the same as in MSM in Western countries, while HIV-1C is the dominant clade among the general population in South Africa.10 Thus, simply finding much HIV-1C among the MSM, particularly the gay identified MSM, would be telling.
However, there may be behavioural or other variables that were not assessed in this survey — such as the lack of prevention messages being targeted to the black MSM population in their own languages. Several of the researchers reported that prevention messages are not effectively targeting this population
Prevention, testing and treatment services for MSM
“It is clear, the current HIV response in South Africa does not meet the needs of MSM,” said Dr Metcalf. Her colleague Professor Rispel described some of the challenges MSM have in accessing services from the public sector.
“Although the majority of survey participants, 57%, had used public health services in the past year (most had little choice because they had no private medical aid), only 7% of individuals said that they would prefer to receive HIV prevention services from a government health service rather than from other service providers,” she said.
From the interviews and focus group discussions, the JEMS researchers found that the only services that exist for MSM are usually provided by non-governmental organizations (usually from the LGBT community) — and with limited capacity or resources these services only reach a very limited number of men.
“One of the issues that came through repeatedly — and it also confirms the findings of other studies — is the unresponsiveness generally of health services to MSM. Health workers often display negative and judgmental attitudes and they tailor clinical management almost exclusively towards heterosexuals. This made men very reluctant to use healthcare services, particularly public health services,” said Prof Rispel. “And due to persistent stigmatization of homosexuality, some MSM fear to disclose their sexual practices and sexual identity to health workers.”
This translates in a reluctance to test as well.
One recent and notable exception is the Health4Men service from PHRU, supported by funding from PEPFAR/USAID, the Elton John AIDS Foundation and others. The first Health4Men service opened in the heart of Cape Town’s “gay village” earlier this year. It launched a progressive prevention campaign targeting MSM (http://www.playnice.me/) and then opened a clinic providing MSM-friendly HIV treatment services at Woodstock Hospital in partnership with the Western Cape Department of Health. PHRU plans to expand the Health4Men service to Soweto and Durban, and their work was acknowledged by South Africa’s Deputy-President of South Africa, who described it as a model for future services in her keynote address at the opening of the South African AIDS Conference.
“The responsiveness of the health system - particularly the public health system - must be improved,” said Prof Rispel. “Firstly through educating healthcare professionals to care for MSM and other sexual minorities in a sensitive and non-judgmental manner. I should say that South Africa is of course the only African country where discrimination on the basis of sexual orientation is outlawed in the highest law of the country so there are already legal provisions for these recommendations that we are making. But certainly, some of the aspects in having a more responsive health system, is educating health professionals, revising existing clinical guidelines to address the needs of MSM, looking at outreach services and also providing support and funding to organizations that are already providing services to MSM.”
In addition to expanding efforts to “eliminate the barriers to VCT and treatment for MSM,” PHRU’s Dladla believes there is a need to “strengthen community-building among MSM.” Likewise, Dr Metcalf said “We need to address structural factors and ensure upholding of human rights of MSM in line with our constitution and also address stigma and discrimination.”
Without such efforts, much of the MSM community is likely to remain “hidden” and under-served.
Finally, the JEMS team said that it is critical that the government must take responsibility for ongoing national surveillance of the HIV epidemic among MSM. “It must be coordinated by government and obviously government should draw on the resources of researchers,” said Prof Rispel.
Dr Metcalf added that this surveillance also needs to “assess the extent of the HIV epidemic among larger, more diverse and ‘representative’ sample.”
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