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EPIDEMIOLOGY AND SOCIAL

Sex behaviour of men who have sex with men and risk of HIV in Andhra Pradesh, India

Dandona, Lalita; Dandona, Rakhia; Gutierrez, Juan Pablob; Kumar, G Anila; McPherson, Samc; Bertozzi, Stefano Mb,d the ASCI FPP Study Team

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doi: 10.1097/01.aids.0000163938.01188.e4
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Abstract

Introduction

India was estimated to have 5.1 million persons living with HIV by the end of 2003, one of the highest number for any country in the world [1,2]. The high risk of HIV in men who have sex with men (MSM) has been documented in different parts of the world [3]. Recent limited data from two cities in India have suggested a high prevalence of HIV in small samples of MSM [4,5]. The sex behaviour of 270–299 MSM each in five large metropolitan cities in India [6], and 125 MSM from rural India [7], has recently been reported. However, detailed information on the sex behaviour of a large sample of MSM across a variety of urban–rural locations in any Indian state has not been reported to inform development of prevention programmes [8]. A major difficulty in getting this information is that homosexuality is hidden to a large degree in India both because of cultural norms and because it is illegal [9]. Efforts are ongoing to attempt legalization of homosexuality in India, but these have not been successful so far [10]. There are historical suggestions that MSM have long been part of Indian society [11], and recent studies suggest that the proportion of men in India who are MSM may not be particularly small [5,7]. However, because many MSM in India do not openly acknowledge their sexual behaviour, this has resulted in scanty knowledge about their sex behaviour and its context. Without this knowledge it is difficult to plan effective MSM-related HIV prevention.

We report the homosexual and bisexual behaviour of a large sample of 6661 MSM from 40 geographic sites, across 62 urban and rural locations of various sizes in 13 districts of the Indian state of Andhra Pradesh, to provide information that would assist in assessing the risk of HIV and planning prevention programmes.

Methods

This study was conducted as part of a baseline for the impact assessment of the Frontiers Prevention Project (FPP). The FPP is being implemented by the International HIV/AIDS Alliance with funding from the Bill & Melinda Gates Foundation. The FPP is based on the principle of providing a comprehensive package of interventions in geographically defined sites that are focused on population groups which are key to the dynamics of the HIV epidemic; that is, those who are at the greatest risk of acquiring/transmitting sexually transmitted infections including HIV and who are best placed to ensure that interventions designed in close collaboration with them are effective. The objectives of this baseline study were to document the socio-demographic characteristics and sex behaviour of one such key population – MSM, analyse these data to identify issues that need particular attention for prevention of HIV and other sexually transmitted infections, and compare these baseline data later with a follow-up study to assess the impact of FPP. The methods relevant to this paper are mentioned below.

This study was approved by the Ethics Committees of the Administrative Staff College of India, Mexico's National Institute of Public Health, the International HIV/AIDS Alliance, and by the Indian Health Ministry's Screening Committee, Indian Council of Medical Research, New Delhi, India. Permissions were obtained from the Andhra Pradesh State AIDS Control Society, the agency coordinating HIV/AIDS control activities in the state, to carry out the study.

Sample

Forty geographic sites in 13 districts of the Telangana and Rayalseema regions of Andhra Pradesh state were identified where access to MSM was considered feasible through MSM facilitators and non-governmental organizations having links with them (Fig. 1). Each geographic site consisted of one or more close-by locations (cities/towns/villages) where MSM were accessible. The total number of locations included in the 40 geographic sites were 62, of which 18 were rural and 44 urban of various sizes, according to the Census of India definitions [12]. In these 62 cities/towns/villages, the number of MSM who might be accessible with reasonable effort was estimated in collaboration with MSM facilitators. The total sample for the study at the 40 geographic sites was planned as 6500. This was based on two considerations. One was accessibility to MSM and the other was the ability to detect a significant change in high-risk sex behaviour between the baseline and follow-up studies. In the absence of much available data on MSM in India, the assumptions about risk behaviour rates and its clustering (which would have an effect on the design effect of the cluster sampling strategy) had relatively wide plausible ranges. We, therefore, preferred to err on the side of a relatively large sample size by including the MSM who were accessible to us in most geographic sites with an upper limit of about 320 for a site if more were accessible.

F1-10
Fig. 1:
Sampled geographic sites.

Data collection

The data collection instruments were developed by an international team with a multidisciplinary background through review of worldwide literature, focus group discussions and in-depth interviews with MSM for the local context in Andhra Pradesh, and pre-pilot studies, to capture a variety of issues related to the sex behaviour of MSM, its socioeconomic context, and awareness about HIV and sexually transmitted infections. An international technical advisory group made suggestions regarding the refinement of instruments. The instruments were translated into the local language Telugu, and the translation was checked through back-translation into English. Extensive training of the interviewers was done by a variety of survey experts and MSM in order to address the technical and ethical issues as well as to promote cultural sensitivity.

Data were collected between July 2003 and April 2004. At each study location (city/town/village), MSM facilitators helped contact and recruit MSM respondents at parks, bus and rail stations, movie theatres, small informal restaurants, and some other places. The eligibility criteria for participation in the study were men more than 15 years of age who had had sex with a man within the past 12 months. Standardized procedures were established and followed for contacting and interviewing respondents. Written informed consent was obtained from each respondent. One-to-one interviews were done confidentially and the identity of respondents was not recorded so that they could not be linked with the data. The data collection process in the field included supervision of the work of interviewers by a quality control supervisor and a field manager in each of the two teams.

Statistical analysis

Data were entered in an LSD (Sistemas Integrales, Santiago, Chile) database. All data entries made by each data entry operator were checked fully by other operators, and any errors found were corrected. The main outcome variables assessed in the analysis were unprotected anal sex with men, unprotected vaginal/anal sex with women, and unprotected sex with both men and women. The 95% confidence intervals (CI) of the estimates for these variables were adjusted for the design effect of the cluster sampling strategy. The design effect is a measure of clustering of a variable, a higher design effect implying higher clustering, and is based on the variation between the clusters for the estimate of that variable [13]. Association of some potential predictor variables with the outcome variables were assessed using multiple logistic regression models to identify those having high odds of unprotected sex, and therefore implicitly with high risk of acquiring or transmitting HIV. In each multiple logistic regression model, the effect of each multi-categorical variable was assessed by keeping the first or the last category as reference, and all variables were introduced simultaneously in the model. The reasons mentioned by MSM for not using condom were assessed to identify barriers to condom use that need to be addressed in the HIV prevention programmes. Statistical analyses were done using SPSS (SPSS Inc, Chicago, Illinois, USA) software.

Many socio-demographic and other variables, the effect of which was assessed on unprotected sex, are self-explanatory. The two that need explanation are ‘knowledge that HIV can be prevented’ and ‘social support score’. Those who responded that they had heard of HIV/AIDS, were asked if HIV infection could be prevented. Those who responded yes to this were considered to have knowledge that HIV could be prevented. Those who responded no and those who had not heard of HIV/AIDS were considered not to have knowledge that HIV could be prevented. The social support score for each respondent was an average of the scores for responses to five questions, which asked if the respondent could count on someone for money, going to doctor, talking about problems, food or place to stay, and abuse; the score for each response ranged from 1 to 5, with 1 indicating least social support and 5 indicating maximum social support.

Results

Of the 7275 MSM contacted for this study across the 40 geographic sites, 6661 (91.6%) participated. The age range of MSM was 16–65 years with the median 27 years. A total of 3059 (45.9%) reported that they were receptive MSM, 2879 (43.2%) insertive MSM, and 723 (10.9%) both. Of 6661 MSM, 609 (9.1%) reported that they were sex workers; 153 (2.3%) were currently married to a man in a private ceremony although same-sex marriage is not legally recognized in India, and 248 (3.7%) were previously married to a man; 409 (6.1%) were currently living with a man sex partner; 2785 (41.8%) were currently married to a woman; 312 (4.7%) were separated/divorced from a woman; and 84 (1.3%) were widowed. A total of 2761 (41.5%) had children.

The sample per geographic site ranged from 72 to 321. It was spread over 62 locations, which included rural villages as well as urban towns/cities of various sizes (Table 1).

T1-10
Table 1:
Distribution of rural–urban locations from which men who had sex with men participated in the study, and their non-use of condom, in Andhra Pradesh, India, 2003–2004.

Sex between MSM

In the last 7 days, of the total 6661 MSM, 4243 (63.7%) had anal sex with at least one man, which included 1026 (15.4%) who also had oral sex, and another 199 (3%) had oral sex with at least one man without having anal sex. A total of 3010 (45.2%) had anal sex with more than one different men in the last 7 days (Table 2). Furthermore, 5782 (86.8%) had sex with at least one man in the last 4 weeks, including 4204 (63.1%) who had sex with three or more different men in the last 4 weeks (Table 2). The mean of the different men sex partners in the last 4 weeks for all MSM was 6 and the median was 4.

T2-10
Table 2:
Number of different men sex partners of 6661 men who had sex with men (MSM) in Andhra Pradesh, India, 2003–2004.

A total of 2139 (32.1%) MSM reported never having used condom. In the last three sex encounters of the 6661 MSM with men, anal sex was performed at least once by 6121 (91.9%) and oral sex at least once by 1592 (23.9%). In addition, 3423 of 6121 MSM (55.9%; 95% CI, 51.7–60.1; design effect 11.2) reported not using condom for anal sex in at least one of their last three encounters with men. This ranged from 39.8 to 64.9% in the various urban–rural location categories (Table 1). Multiple logistic regression revealed that lack of knowledge by MSM that HIV can be prevented was most strongly associated with this non-use of condom (odds ratio 8.80; 95% CI, 7.55–10.25); the other variables associated significantly with non-use of condom are shown in Table 3. The interactions between the following variables were found significant in determining either no or inconsistent use of condom: knowledge that HIV can be prevented and rural–urban area where the MSM was sampled from (P < 0.001, negative interaction), knowledge that HIV can be prevented and education level of MSM (P = 0.002, negative interaction), and rural–urban area where the MSM was sampled from and education level of MSM (P = 0.001, positive interaction).

T3-10
Table 3:
Multiple logistic regression for associations with non-use of condom for anal sex by men who have sex with men (MSM) in their last three sex encounters with men and also for vaginal/anal sex with woman in last sex encounter.

Details about the type of sex and the use of condom and lubricants were available for 19640 sex encounters (Fig. 2). Anal sex was performed in 85.4% of the encounters, of which condom was not used in 47.4% encounters. The use of safe water-based lubricant with a condom was extremely rare. Of the encounters in which there was no anal sex, oral sex was performed in 48.6%, of which 17.6% were with condom. Of the 1476 (7.5% of total) encounters in which there was no anal or oral sex, thigh sex (using upper portion of thighs as receptacle without anal penetration) was performed in 1019 (69%) and masturbation in 722 (48.9%) – these were not mutually exclusive.

F2-10
Fig. 2:
Anal and oral sex, and use of condom and lubricant, in 19 640 sex encounters between men in Andhra Pradesh, India, 2003–2004. MSM, men who have sex with men.

Among the 4454 MSM who had ever used condom, 1158 (26%) reported that they had experienced condom breakage during sex.

Sex between MSM and women

Of the 6661 MSM, 4553 (68.4%) had ever had sex with a woman. A total of 3364 (50.5%) had sex with a woman in the last 3 months, including 2200 (33%) who had sex with one woman, 637 (9.6%) with two women, 422 (6.3%) with three to five women, and 105 (1.6%) with more than five women. Of the 3364 MSM who had sex with a woman in the last 3 months, 2534 (75.6%) reported having sex with wife, 966 (28.7%) with woman sex worker(s), and 430 (12.8%) with wife as well as woman sex worker(s). The last sex with a woman by these 3364 MSM included vaginal sex by 3346 (99.5%), anal sex by 75 (2.2%), and oral sex by 100 (3%) – these were not mutually exclusive. Of the 3354 MSM who reported vaginal or anal sex, 2818 (84%; 95% CI, 81.1–86.9%; design effect 5.6) did not use condom for this.

Of the 6121 MSM who reported anal sex in the last three sex encounters with men, 1585 25.9%; 95% CI, 22.7–29.1; design effect 8.4) reported not using condom for anal sex in at least one of these encounters and also reported having vaginal/anal sex without condom with the last woman sex partner in the past 3 months. This ranged from 17.2 to 32.8% in the various urban–rural location categories (Table 1). Multiple logistic regression showed that these MSM had remarkably high odds of being currently married to a woman (15.3; 95% CI, 12.6–18.4) and there was significant association with some others variables as well (Table 3). There was significant positive interaction between marital status with woman and reported type of MSM in determining non-use of condom with both men and women (P < 0.001).

Barriers to condom use

The reasons given for not using condom by the 2632 MSM, who had anal sex in the last sex encounter with a man and did not use condom, included a wide variety (Fig. 3). Of the 2818 MSM who did not use condom for the last vaginal/anal sex with a woman, the predominant reason given was ‘do not use with regular partner’ (Fig. 3).

F3-10
Fig. 3:
Reasons given by men who have sex with men for not using condom for anal sex with men ( n = 2632) and for vaginal/anal sex with women ( n = 2818) in last sex encounter. The total percentage for the reasons for not using condom with men, and for women, both exceed 100 as some respondents gave more than one reason.

Discussion

Detailed data on the sex behaviour of MSM and interventions to reduce risk of HIV related to this are accumulating from high-income countries [3,14–16],but such data are not readily available from India to inform development of HIV prevention programmes. This study documents in a large sample of 6661 MSM from rural and urban locations of various sizes, in 13 districts of an Indian state, that over half of the MSM reported not using condom for anal sex with men and about a quarter reported not using condom both for anal sex with men as well as for vaginal/anal sex with women. This suggests a high risk of transmitting/acquiring HIV among this sample of MSM and their women sex partners, especially wives.

Some limitations of this study have to be considered while interpreting these data. The MSM recruited in this study were those who were accessible through MSM facilitators, indicating that this sample would have very likely included the relatively more active and visible MSM, and would not be representative of the entire MSM community in this Indian state. In addition, it is generally felt that some/many receptive MSM may self-report themselves as insertive, and therefore, the reported distribution in this sample may not be fully accurate. Moreover, behavioural surveys carry the risk of over-reporting of desirable behaviour by the respondents [17,18], which applies to this study too, indicating that the actual condom use rates may be even lower than reported. On the other hand, there is also a chance that some MSM may have over-reported their high-risk sex behaviour, as this may be perceived by them to be adventurous. Even with these limitations, these data still indicate two broad trends that cannot be ignored. First, there are MSM in rural and all sizes of urban locations in India who have penetrative sex with multiple men and use condom infrequently, putting them at high risk of acquiring/transmitting HIV. Second, the wives of these MSM are at particular risk of HIV across the range of rural–urban locations, as the vast majority have unprotected sex with their husbands. It would be useful to take these two messages into account while developing HIV prevention programmes in India.

The finding of this study that knowledge that HIV can be prevented was the strongest predictor of use of condom for anal sex among MSM in multivariate analysis indicates the central role that this modifiable factor can potentially play in HIV prevention programmes. Some demographic associations found with non-use of condom among MSM, namely lower education, lower income and higher age, could be used to identify those who are at relatively higher risk. In addition, those MSM having medium range of men sex partners (two to five in the last 4 weeks) had relatively higher risk of not using condoms than those with a higher number of sex partners. Lower social support score in this study, a relatively crude indicator of one aspect of social capital [19], was also associated with higher risk of not using condom. The use of safe water-based lubricants for anal sex was reported to be almost non-existent, which indicates that this needs to be addressed along with condom use in HIV prevention programmes in India, as there is higher risk of condom breakage in anal sex without use of safe lubricants [20]. About a quarter of those who reported not using condom for anal sex were not aware of condom, and the remaining gave reasons for this non-use ranging from not liking condom to favourable partner characteristics, indicating that a multitude of factors need to be addressed in overcoming the barriers to condom use for anal sex by MSM in India.

Half of the MSM had had sex with at least one woman in the last 3 months. Although the largest proportion among these women were wives, 29% of the MSM who had sex with women in this period had had sex with woman sex worker(s), including 13% who had sex with their wife and with women sex worker(s). By far the strongest association of having unprotected penetrative sex with both men and women in multivariate analysis was with MSM married to a woman. The predominant reason reported for not using condom with women was that they do not use them with regular partner, which was reported by over two-thirds. A previous survey of 270 to 299 MSM each from five large metropolitan cities in India had reported that about one-third of MSM had had sex with women in the past 6 months [6]. The present study on a larger number of MSM in various sizes of urban and rural locations indicates that this proportion may be even larger and that such bisexual behaviour is widely prevalent across the urban–rural locations. These data suggest that HIV prevention programmes among MSM in India not only need to work on increasing correct and consistent condom use for sex among MSM but also for sex by MSM with their women partners, especially wives, in a range of urban–rural locations and not only in large cities. This is a complex issue, as it also relates to gender equations in sexuality in India, but nevertheless it cannot be ignored if comprehensive MSM-related HIV prevention programmes are to be evolved in India.

Large comprehensive studies assessing the extent of homosexuality are not readily available from India. One recent study reported that 5.9% of 774 men in the slums of the metropolitan city of Chennai had ever had anal or oral sex with a man [5], and another study of 2910 men from five rural districts of India reported that 9.5% of single men and 3.1% of married men had had anal sex with a man in the past year [7]. Although large studies are needed to get a better understanding of these estimates, these data suggest that the proportion of men who have sex with men may not be very small in India. Homosexuality in India, as in some other nations, is considered illegal [9,21]. This is inter-related with poor acceptance of homosexuality by Indian society [10] and is a sensitive issue, made more complex because of the general tendency in India not to openly discuss sexuality. However, the findings of this study on a large sample of MSM that high-risk sex by MSM among themselves and with their women sex partners is prevalent in a wide range of rural and urban locations in this Indian state, and is not limited only to large cities, underscores the need to pay adequate attention to homosexuality/bisexuality and its implications for HIV control in India.

The quantitative data from the study reported in this paper have highlighted some major issues that need to be addressed as part of the MSM-related HIV prevention in India. These data are being utilized by FPP to improve the prevention package being developed and implemented. However, substantial further work is needed to understand the nuances of MSM behaviour in India. Such work, through well-designed qualitative and quantitative studies, must look at the social and cultural context of the MSM behaviour in India [22,23], which would help to provide a better understanding of how HIV prevention would actually work. Efforts to establish an adequate evidence-base regarding homosexuality/bisexuality in India are especially important for developing effective HIV prevention because efforts historically have been so focused on heterosexual transmission. This would form an important element of the comprehensive evidence-base needed to control HIV/AIDS in India [8,24].

Acknowledgments

We thank the many MSM who participated in this study, the MSM facilitators, and the non-governmental organizations, the Andhra Pradesh State AIDS Control Society, the International HIV/AIDS Alliance and India HIV/AIDS Alliance for supporting and facilitating this study. The opinions expressed in this paper are those of the authors and do not necessarily reflect the views of the funding agency or the other organizations that supported and facilitated this study.

Sponsorship: The Frontiers Prevention Project, including this study, is supported by a grant from the Bill and Melinda Gates Foundation.

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Appendix 1

The members of the ASCI FPP Study Team other than the named authors include (in alphabetical order):

G. Md. Mushtaq Ahmed, Md. Akbar, Md. Abdul Ameer, Ch. Arjun, N. Arjun, M. Sai Baba, C. Satish Babu, J. Kishore Babu, I. Balasubrahmanyam, V. S. Udaya Bhaskar, T. Gangadhar, P. Gopal, Lavanya Gotety, Shaik Omar Hussain, V. Indira, S. Krishna, P. Kiran Kumar, Ch. Sri Jaya Lakshmi, T. Uma Maheshwar, P. Chandra Mouli, S. Radhakrishnan, K. Raghu, S. P. Ramgopal, A. Srinivas Rao, A. Srinivasa Rao, K. Hanumantha Rao, N. Ananda Rao, P. Venkateswara Rao, Parsa V. R. Rao, D. Ravinder, A. Srinivas Reddy, G. Brahmananda Reddy, S. Krishna Reddy, G. Uma Sankar, A. Satyam, Y. S. Sivan, P. V. Sridhar.

Keywords:

anal sex; bisexuality; condom; HIV; homosexuality; India; men who have sex with men

© 2005 Lippincott Williams & Wilkins, Inc.