An exploration of elevated HIV and STI risk among male sex workers from India

In the first decade of 2000, HIV prevalence among men who have sex with men (MSM) increased in many countries across the world [1–5]. HIV prevalence estimates computed using pooled data from seven Asian countries (Thailand, Vietnam, Cambodia, China, Indonesia, India and Nepal), found that MSM are 19 times more likely to get infected than other men of reproductive age [1]. MSM are particularly vulnerable to HIV because of their wide range of HIV-related risk behaviours including high number of sexual partners, bisexual behaviour, inconsistent condom use, substance use, transactional sex, and low levels of awareness on HIV and sexually transmitted infections (STIs) [6, 7]. Studies conducted among MSM in low and middle-income countries have demonstrated that HIV risks are associated with a variety of sexual partnerships and sexual practices [2, 8]. In India, MSM who sell sex (male sex workers or MSWs) have a greater risk for HIV and STIs than other MSM [9–11]. MSWs are more vulnerable to HIV than other MSM because MSWs need to fulfil the desires of their clients and, in some instances, agree to unprotected sex, particularly when there is a scarcity of clients [12]. While MSWs may serve as HIV core transmitters to their clients, they may also function as a bridge group in the transmission of HIV and other STIs to the general population because they also engage in non-commercial sex with male and female partners [13].

Even though male to male sex has recently been decriminalized in India, social stigma may hinder risk-reduction and access to HIV prevention interventions [14]. Programme data from 2006 estimated that there were 20,800 high-risk MSM in Mumbai and 5,000 in Hyderabad [15]. Using the proportion of self-reported transactional sex in the 2007 surveillance survey among MSM, the numbers of MSWs are estimated to be 7,700 in Mumbai and 1,800 in Hyderabad [16].

The Indian National AIDS Control Programme has recognised the importance of HIV prevention for MSM and supports NGOs providing targeted interventions for high-risk MSM (HR-MSM), defined as MSM with multiple sexual partners [17]. However, the interventions are uniform for MSM, male-to-female transgendered persons (TGs) and MSWs [17]. The prevention package includes peer-led outreach education, promotion and distribution of condoms and lubricants, STI clinical services, community mobilization and structural interventions. STI clinics provide services for management of STI syndromes, periodic STI check-ups and syphilis screening. Additionally, HIV voluntary counselling and testing (VCT) services are provided either on-site or through referrals.

This study presents the socio-demographic characteristics and HIV/STI prevalence of MSWs. The authors investigate the factors associated with HIV infection among MSWs and highlight the need for tailored services for this population.

A cross-sectional study was conducted during 2008–2009 in four dedicated MSM clinics, run by NGOs implementing HIV prevention programmes for HR-MSM and TGs. The clinics were located in Mumbai and Hyderabad, two large cities in India. Eligible participants were MSM clinic attendees aged 18 years or more, who reported having had sex with at least two male partners in the last month and were not under the influence of alcohol or drugs at the time of consultation. MSM were mobilized to participate in the study by peer educators through the outreach. However, all clients attending the clinics during the study period were screened for eligibility. Informed consent was administered to eligible MSM. Participants received a compensation corresponding to the cost of transport to the clinic. The study protocol was approved by the institutional ethical review committees of the National AIDS Research Institute (NARI) of India and the FHI 360 Protection of Human Subjects Committee in the USA. All staff was trained on study procedures.

A total of 551 eligible MSM were contacted for the study, of them 22 refused participation. Of the 529 enrolled study participants, 17 had incomplete data (either behavioural or biological). Among the 512 MSM with complete data, 29 TGs were excluded from the present analysis. The 483 MSM retained for analysis included 326 (67%) from Hyderabad and 157 (33%) from Mumbai.

Our study showed that MSWs reported more HIV risk behaviours in comparison to other MSM, including a higher number of male sexual partners, a higher proportion reporting substance use and receptive anal sex, and a lower proportion accessing STI services. The prevalence of HIV and HSV-2 among MSM in general, and MSWs in particular, was high. HIV prevalence among MSWs was associated with the place of residence (higher in Hyderabad than Mumbai), HSV-2 and syphilis seropositive status and duration of sex work. Our survey also found a very high HIV prevalence of 57% among MSWs who had sold sex for more than 10 years. As the duration in sex work increased, MSWs were less likely to report insertive anal sex and more likely to self-identify as kothis/engaging in receptive anal sex. As compared to Mumbai, MSWs from Hyderabad were at higher risk for HIV possibly owing to several factors; they were older, a higher proportion were selling sex, reported higher rates of receptive anal sex and substance use, and had a higher prevalence of curable STIs.

The prevalence of HIV among MSM in our clinic-based study is substantially higher than the prevalence estimates obtained from a community-based study in 2009, the Integrated Behavioural and Biological Assessment, Round 2 (IBBA-2) that selected participants through time-location cluster sampling. However, the IBBA-2 also showed a higher HIV prevalence among MSM in Hyderabad than in Mumbai (25.8% and 3.8% respectively) [18]. Another study, conducted among MSM in the twin cities of Hyderabad and Secunderabad, which used a non-randomly generated sample from drop in centres and pubic cruising sites, reported an HIV prevalence of 22%; the multiple logistic regression analysis showed significant associations of seropositivity with age (>30 years), educational level (lower among post-graduates), history of unprotected anal intercourse and reported sexual positions (both unmarried and married receptive/kothis and unmarried dual/double deckers) [19]. Hyderabad and Mumbai are the capital cities of the states of Andhra Pradesh and Maharashtra respectively. The 2010–11 National HIV Sentinel Surveillance (HSS) showed that the HIV prevalence among pregnant women (used as a proxy for the general population) in the state of Andhra Pradesh is much higher than that of Maharashtra and the national average (Andhra Pradesh 0.76%, Maharashtra 0.42%, national average 0.40%) [4]. While the multivariate analysis for HIV seropositivity in our study included well-known individual risk factors, it is possible that the higher risk in Hyderabad may also be driven by other factors not measured such as a higher exposure to HIV through sexual networks of partners who have a higher HIV prevalence.

The prevalence of HSV-2 among MSWs (60%) is considerably higher than that among general male population in India (10%) [20]. As compared to MSM not selling sex, the high prevalence of HSV-2 among MSWs is consistent with their higher number of male partners, since HSV-2 in MSM is strongly associated with the number of lifetime sexual partners [21].

Reported consistent condom use was relatively low with non-commercial male partners and very low with female partners. MSM’s reported condom use at last sex was lowest for anal sex with female partners, which is consistent with studies showing that many MSM do not consider anal sex as a risk behaviour [22, 23]. Almost half of the MSWs reported having sex with women and a small proportion also reported sex with female sex workers. In India, many MSM get married and engage in marital sex in response to familial and peer pressures, as well as social and cultural norms [24, 25]. Our data also shows a rising trend of a 'currently married’ status among MSWs with an increasing duration in sex work. MSWs who have been selling sex for longer periods may play a substantial role in transmitting HIV to their wives and other female sexual partners because of high HIV prevalence and risky sexual practices.

Despite the fact that one out of four MSWs was infected with curable STIs, only a few perceived themselves at risk for STIs and a quarter had never visited the program clinic for STI services prior to the study. This gap in uptake of clinical services needs to be addressed. It is known that clinic visits provide opportunities for risk-reduction counselling, STI management, syphilis and HIV testing. A study among MSWs in Mumbai showed that HIV positives are 2.4 times more likely to be co-infected with life-time syphilis [11]. Our study also found a relatively high prevalence of syphilis among MSWs, which is alarming as syphilis was found to be a significant co-factor for HIV prevalence in our sample.

A majority of the MSM and more of the MSWs reported consuming alcohol or drugs. It has been demonstrated that substance use may be a mechanism used by MSM to cope with psychosocial pressures [26]. In Pakistan, for example, it is the MSWs’ daily preoccupation to conceal sex work activities and homosexuality from their families and a stigmatizing society [27]. Alcohol/drug use among MSM in India was found associated with high risk sexual behaviours, improper use of condoms and poor condom use negotiation [28].

There were several limitations in our study. Since the study was conducted in targeted intervention clinics, the participation of MSWs in our study could be disproportionately high and the prevalence of HIV/STIs and correlates may be different in MSM/MSWs who do not attend such facilities. Therefore, our results may not represent the general population of MSM/MSWs in the two cities. The small sample size of some subgroups/categories of MSWs may affect the statistical power of estimates and hence there is a need to interpret the data with caution. However, we have presented the analysis as there are limited studies on the risk characteristics of MSWs and they are an important group for HIV prevention. We did not collect data on prior HIV testing, which limits our understanding of MSWs possible uptake of treatment services. Finally, because this was a cross-sectional assessment, we cannot make causal inferences.

Our study found that MSWs are extremely vulnerable to HIV and are likely to be core transmitters to their male and female partners, which highlights the need for intensified interventions for MSWs. Outreach workers should prioritize MSWs for prevention services through intensified risk-reduction education and promoting regular clinic visits. Clinical services should focus on periodic syphilis and HIV screening, personalized risk-reduction counselling including condom negotiation skills. Marital and regular partners of MSWs are also at high risk for HIV infection. Hence, effective mechanisms for partner management need to be established. Given the high HIV prevalence and vulnerability of MSWs, studies on the feasibility and acceptability of the newer bio-medical interventions such as pre-exposure prophylaxis and treatment as prevention could be considered.