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Sexual Risk Taking, STI and HIV Prevalence Among MenWho Have Sex with Men in Six Indonesian Cities Guy Morineau Æ Naning Nugrahini ÆPandu Riono Æ Nurhayati Æ Philippe Girault ÆDyah Erti Mustikawati Æ Robert Magnani Ó Springer Science+Business Media, LLC 2009 Using surveillance data on men who have sex condom and lubricant use, prevention efforts must also with men (MSM) from six Indonesian cities, this article reports prevalence of sexual risk taking, HIV and othersexually transmitted infections. Factors associated with HIV, other STIs and consistent condom use were assessed.
Behavioral data were collected from 1,450 MSM, amongwhom 749 were tested for HIV and syphilis and 738 forgonorrhea and Chlamydia. Associations were assessed using multivariate logistic regression. Over 80% of MSMknew HIV transmission routes, 65% of MSM had multiple With the exception of Papua and West Papua Provinces on male sexual partners, 27% unprotected anal sex with the island of New Guinea, where a low-prevalence gen- multiple male partners, and 27% sex with a female in the eralized HIV/AIDS epidemic has emerged (population prior month. Consistent condom use ranged from 30 to prevalence = 2.4%), HIV/AIDS in Indonesia remains 40% with male partners and 20 to 30% with female part- concentrated in certain ‘‘most-at-risk-groups’’ While ners, depending upon partner type. HIV prevalence aver- the HIV/AIDS epidemic in Indonesia has been driven aged 5.2%, but was 8.0% in Jakarta. Prevalence of rectal primarily by the sharing of contaminated drug injecting gonorrhea or Chlamydia was 32%. Multivariate analyses equipment since the late 1990s, it is currently believed that revealed recent methamphetamine use and current rectal the role of injecting drug use in driving HIV/AIDS may be gonorrheal or chlamydial infection to be associated with peaking or have already peaked []. Indeed, the Indo- HIV infection. The data confirm diverse sexual networks nesian National AIDS Commission projects that between and substantial sexual risk-taking, despite relatively high 2007 and 2027 men who are infected via unprotected sex levels of education and HIV-related knowledge. In addition with female sex workers and with other men will account to promoting partner reduction and more consistent for the majority of new HIV infections These projec-tions are consistent with those of the Commission on AIDSin Asia for the region as a whole Responding to an expanding HIV/AIDS epidemic G. Morineau (&) Á P. GiraultFamily Health International, Asia/Pacific Regional Office, among men who have sex with men (MSM) presents a 19th Floor, Sindhorn Building, Tower 3, 130 -132 Wireless Rd, formidable challenge in Indonesia for several reasons. First and foremost is that the epidemic is occurring in a context of stigma and discrimination, resulting in many MSM remaining ‘‘hidden’’ and thus difficult to reach with Sub-Directorate for HIV/AIDS & STIs, Ministry of Health, information and services in a systematic way. This is Republic of Indonesia, Jakarta, Indonesia compounded by a limited evidence base concerning num-bers of MSM, their risk-taking and health-seeking behav- P. Riono Á Nurhayati Á R. MagnaniFamily Health International, Jakarta, Indonesia iors, and infection rates. Aside from limited behavioral questions for small samples of MSM included in behavioral groups and local health authorities. Survey subjects were surveillance surveys conducted in 2002–2003 [] and selected via two-stage, time-location sampling (TLS). At 2004–2005 ], the only other available behavioral data the first stage, locations were randomly selected with come from qualitative studies with uncertain generaliz- probability proportional to the estimated number of men at ability [, Biological data (i.e., HIV and STI prevalence each location. A sample of MSM of size proportional to rates) are yet scarcer. Transgenders (i.e., ‘‘Waria’’) in venue size was then selected via systematic-random sam- Jakarta were included in Ministry of Health sentinel sur- pling. All selected MSM were asked to voluntarily par- veillance through 2005, and the MOH undertook a small ticipate in a behavioral survey using a structured study of MSM in which HIV and syphilis prevalence was questionnaire, and in Jakarta and Surabaya provide bio- measured for a sample of 750 MSM in Jakarta [, but surveillance otherwise has not covered MSM. The Ministry In Batam, Bandung, and Malang, MSM were recruited of Health estimated that there were about 767,000 MSM in through respondent driven sampling (RDS). Eight MSM the country as of 2006 (range 385,000–1,150,000) [ ‘‘seeds’’ were recruited purposively in each city, ensuring This paper takes advantage of biological and behavioral that they (1) lived in the city, (2) were aged 15–49, and (3) surveillance data gathered from MSM in six Indonesian were part of an extended network of MSM. All seeds and cities in the 2007 Integrated Biological-Behavioral Sur- subsequent recruits were each given three (3) coupons to veillance (IBBS) surveys to assess the current epidemiologic recruit other MSM they knew. Recruiters received US$ 4 for situation among MSM and determine factors associated with each successful recruit. The survey was terminated when the HIV and other STI infection. The IBBS represent the first target sample size was reached in each city. Recruits in large-scale, systematic data collection in Indonesia for this Bandung were asked to provide biological samples.
important sub-population with both behavioral and biologi- The use of different sampling methods was part of the cal data. These data are timely in that if, as has been sug- process of developing a surveillance system for MSM. In gested by the projections cited above, HIV/AIDS in the 2007 IBBS, RDS was tried as an alternative to TLS in Indonesia is evolving such that sexual transmission among the smaller cities to assess its advantages in reaching more MSM will play a more significant role in future transmission, ‘‘hidden’’ MSM. The results will be used to assess and it is crucial that national health authorities understand the guide choice of sampling methods for MSM in future current realities so that appropriate action can be taken.
Survey field teams were drawn from staff of provincial offices of the Central Statistics Bureau, provincial healthdepartments, and CBOs and NGOs serving MSM in the Behavioral survey data were collected from independent survey area. Survey staff received specialized training on samples of 1,450 MSM in six Indonesian cities between survey field procedures. In as private a location as could be August and November 2007. The cities included Bandung found, interviewers explained the study procedures, sought (West Java), Jakarta, Malang (East Java), Medan (North informed consent and gathered behavioral survey data Sumatra), Semarang (Central Java) and Surabaya (East using structured, pre-coded questionnaires. A nurse col- Java). MSM interviewed in Bandung, Jakarta and Surabaya lected blood through finger prick, and participants provided were asked to provide biological samples, and 749 men self-collected rectal swabs and first-void urine. Behavioral were successfully tested for HIV, syphilis, and urethral and biological data were gathered anonymously and were Chlamydia and gonorrhea, and 738 for rectal Chlamydia linked via special ID numbers. Participants received a and gonorrhea. MSM were defined as men who have sex coupon for free HIV counseling and testing at a nearby with other men either for commercial gain or as a matter of Community Health Center and were given their participant sexual preference. Data were also obtained from indepen- number in order to access their STI test results and receive dent samples of transgenders, but as the underlying treatment free of charge if needed. Laboratory methods.
dynamics of the HIV/AIDS epidemic among transgenders Blood specimens were collected in EDTA tubes, stored differ markedly from MSM as defined above, they are not at 4–6°C and transported to a government provincial lab- oratories within five hours to be tested for HIV and syph- In Jakarta, Surabaya, and Medan, sampling frames were ilis. HIV was tested using two rapid tests conducted in developed from mappings of locations where MSM could parallel: SD Bioline HIV 1/2 3.0Ò (Standard Diagnostic, be found. These were produced jointly by non-govern- Korea, South Korea) and DetermineÒ HIV-1 (Abbott, mental organizations (NGOs) providing services to such Abbott Park, IL). Discrepant results were re-tested at the National Reference Laboratory using two ELISA: MurexÒ held salaried position at the time of the survey, with HIV 1.2.0 (Murex Biotech, Dartford, UK) and Vironosti- another 26% being independent workers/performing odd kaÒ HIV-1 Plus O (Biomerieux, Marcy l’Etoile, France) jobs. Nine percent worked in a salon/beauty parlor, which and results that remained discordant were classified as often serve as men to men sex trade locations. Only 11% of indeterminate. Syphilis was tested using a treponemal test: MSM had resided in the city in which they were inter- Determine Syphilis TPÒ (Inverness Medical, Bedford, viewed for 1 year or less, whereas 58% had lived in their UK). Rectal swabs and urine specimens were tested for current city of residence for 10 years or more and 41% Chlamydia and gonorrhea via PCR using Cobas AmplicorÒ As shown in Table , differences in background char- acteristics of MSM sampled via TLS were significantly different (P \ .05) from those sampled via RDS on five ofthe six characteristics considered. However, although sta- Behavioral data were double entered using CSPro 2.6.007 tistically significant, the differences are not pronounced (US Census Bureau). Laboratory data were entered using enough to preclude combining the two samples. Further- Microsoft Excel. Analysis was performed using Stata 9.0 more, the only background characteristic on which there (Stata Corporation, College Station, TX). The implications was not a significant difference depending upon sampling of use of two different sampling methods were assessed by method, level of education, was the only characteristic comparing background characteristics of respondents by found to be significantly associated with any of the out- type of sampling methodology. Subsequent analysis was come variables in multivariable analyses. Consequently, all performed on multisite pooled data, assuming a stratified analyses were undertaken with the full sample of MSM.
simple random sampling design. Simple logistic regressionwas used to assess associations of background character- Knowledge of HIV/AIDS-related Risk and Protective istics and risk behaviors with three separate outcomes: HIV, rectal infection with Chlamydia or gonorrhea, andconsistent condom use in anal sex with male partners in the MSM included in the IBBS were knowledgeable about past month. Differences were assessed using the Wald test, HIV/AIDS (data not shown). Knowledge questions that and P values of \ 0.05 were considered significant. Mul- were correctly answered by over 80% of MSM included: tivariate logistic regression was used to determine the net protection offered by condoms from transmission of HIV contributions of factors that were significant at the P B .20 during vaginal and anal sex; HIV transmissibility via level or better in bivariate analyses. Factors were elimi- sharing of contaminated drug injecting equipment, during nated in a backward stepwise elimination process based the course of child birth, and through breastfeeding infants; upon their contribution to variance explained until only and that it was not possible to recognize HIV-infected factors significant at the P \ .05 level remained in the final persons by their appearance. However, 41% thought HIV transmission could be prevented by taking antibioticsbefore having sex and 27% believed that HIV could betransmitted through sharing food utensils.
Sexual Activity and Other Risk-taking Behaviors The initial sex partner of most MSM (66%) was another Respondent background data are displayed in Table male, although 32% reported first sex with a female and separately for MSM sampled via time-location sampling 2% with a transgender (not shown). Mean age at first sex (TLS) versus respondent-driven sampling (RDS). In the was 18.2 years (Table Nearly 63% of MSM had ever aggregate, respondents averaged just over 28 years of age.
bought or sold sex, with a mean duration of almost 7 years Although most MSM were never married (to a female), since first commercial sex. Ten percent reported ever 15% were currently and another 5% were formerly mar- having been forced into sex. Fifty-seven percent of men ried. The most common living arrangement was with reported having a regular sex partner at the time of the family (i.e., parents and/or siblings; 44%), with another survey interview, two-thirds of whom were male.
26% living alone and 19% living with friends. Six percent The data on sexual partners in the year prior to the lived with a regular female partner and 5% a regular male survey indicate both volume and diversity. Most MSM had partner. Education levels were relatively high, with 58% of sex with a casual male partner in the prior year and over respondents having attended senior high school and another one-half with a regular male partner; that is, a partner in a 24% college/university. A large proportion of MSM (45%) long-term relationship as defined by the respondent. Selling characteristics of MSM in sixIndonesian cities sex to other MSM was more common than buying sex from Nearly 35% of MSM had received an STI check-up at a MSM. A sizeable proportion of respondents also had sex clinic in the 3 months prior to the survey, reflecting recent with females during the reference year—most often with efforts in Indonesia to promote routine check-ups among casual female partners, but 14% also sold sex to and 10% sexually active MSM. Approximately 25% of respondents bought sex from females during the previous year.
reported having had STI symptoms in the prior year. Of Sexual partners in the month prior to the survey were those, less than half received professional medical treat- also diverse, but were dominated by casual male partners, ment, more often from private—than public-sector service male clients and casual female partners. Seventy-five per- providers. A plurality of MSM (36%) either self-treated or cent of MSM had sex with a casual male partner in the sought traditional treatment, while 20% of cases went prior month, with a mean of 2.8 partners. Thirty-five per- untreated. About 40% of men had ever been tested for HIV, cent of MSM sold sex to a male client in the previous the large majority in the previous year, again likely month with a mean of 6.6 clients (median = 3.0), while reflecting recent expansion of HIV/AIDS program cover- 13% reported buying sex from another male. Twenty-six percent of MSM had sex with a casual female partner in thepast month.
Approximately 15% of MSM reported using metham- phetamine before having sex, in the 3 months prior to the Condom use at last anal sex with male partner exceeded 60%, survey. However, methamphetamine use was much higher but was substantially lower at last vaginal sex with female in two cities—Jakarta (31%) and Medan, North Sumatra partners (Table ). With female partners, condom use was more common with commercial than with casual partners, Table 2 Risk-taking and health-seeking behaviors among MSM Heath seeking behaviors at last symptomatic episode of STI (%) with whom condoms were used in only one-third of last sexual episodes. Consistent condom use in the last month was substantially lower, ranging between 32 and 36% with male partners and between 12 and 20% with female partners.
Water-based lubricants were used less consistently than condoms—between 26 and 34% with male commercial and casual male partners, and only 12% with transgender part- ners. Thirty percent or less of MSM, depending upon partner type, consistently used both condoms and water-based lubricants during anal sex in the prior month.
Condom use during anal sex appears not to vary depending upon type of male partner, with roughly equal proportions of MSM reporting condom use at last anal sex and consistently in the last month with casual as with commercial partners. Nor does it appear to vary dependingupon whether anal sex was insertive or receptive, as the proportion of MSM who had unprotected insertive anal sex with a male partner in the prior month was identical to the proportion having unprotected receptive anal sex—66% Data on HIV and other STI prevalence for MSM in three cities are displayed in Table HIV prevalence for the full Mean number of partners past month (among those who had this type sample of men was 5.2%, with a high of 8.0% in Jakarta and a low of 2.0% in Bandung. Overall syphilis prevalence was 4.3%, and was the highest in Bandung and lowest in Jakarta. Prevalence of urethral STIs was relatively high, with an average of 6.3% testing positive for either Chla- mydia or gonorrhea. Prevalence of rectal STIs was con- siderably higher—Chlamydia 21%, gonorrhea 19%, and Had routine STI check-up in past 3 months (%) The results of multiple logistic regression analyses under- taken to identify factors associated with HIV-positive Table 3 Use of condom and lubricant by type of sexual partners Always used both condom and lubricant (214) 23.8 NA not available (information not collected) Table 4 Prevalence of HIV and other sexually transmitted infections (STI) among MSM status, presence of other STI infections, and consistent education were associated with increasingly higher likeli- condom use in male-to-male anal sex in the prior month, hood of consistent condom use. MSM who attended senior respectively, are presented in Tables , and With high school were more likely to have used condoms con- regard to the results with HIV status as the outcome vari- sistently than those with junior high level or below levels able, although a number of factors were associated with of education (OR = 1.67; 95% CI = 1.08–2.58), and HIV-positive status at the bivariate level, only two vari- MSM who attended college/university being more than ables retained significant associations in the multivariate twice as likely (OR = 2.16; 95% CI = 1.33–3.52). Other analyses—(1) use of methamphetamines or similar drugs in factors associated with higher likelihood of consistent the prior 3 months (OR = 2.69; 95% CI = 1.33–5.43) and condom use included having sufficient knowledge of HIV (2) Chlamydia or gonorrhea infection at the time of the survey (OR = 2.04; 95% CI = 1.06–3.92; Table (OR = 1.41; 95% CI = 1.04–1.88) and having been tested After accounting for the effects of other factors, four for HIV in the past year (OR = 2.25; 95% CI = 1.66– factors were associated with Chlamydia or gonorrhea infection at the time of the survey—(1) forced into sex in Several factors were associated with reduced likelihood the prior year (OR = 2.21; 95% CI = 1.39–3.50), (2) of consistent condom use. The data indicate that consistent number of casual male partners in the prior month condom use during anal sex declines with increased dura- tion of selling sex, with MSM who had been selling sex tion(OR = 2.41; 95% CI = 1.20–4.84), and (4) having had 2–4 years being 43% less likely to use condoms than men sex with a female partner in the past year (OR = 0.54; 95% who never sold sex, while those who sold sex for 5 years or more were 45% less likely to have used condoms consis- Seven factors were found to be associated with consis- tently. MSM who had sold sex for 1 year or less did not, tent condom use in anal sex in the prior month in the however, differ significantly with regard to consistent multivariable analyses (Table Increasing levels of condom from men who had never sold sex. Use of Number of male casual partners past month Number of commercial male partners past month Number of female casual partners past month Number of commercial female partners past month Always used condom use with male non-regular partners past month Condom use with female partners past month Use of lubricants in anal sex in last month Currently infected with urethral CT or NG with rectal infection withchlamydia or gonorrhea Number of male casual partners past month Number of commercial male partners past month Number of female casual partners past month Number of commercial female partners past month Condom use with casual male partner past month Always used lubricant with casual male past month Always used of lubricant in anal sex past month Condom use casual female partner past month methamphetamines, ecstasy or similar psychostimulants in The final factor associated with reduced odds of con- the prior 3 months was associated with significantly lower sistent condom use was condom use with female partners.
likelihood of consistent condom use (OR = 0.59; 95% MSM who did not used condoms consistently with casual female partners were also less likely to have used condoms with consistent condom use inanal sex past month Know that HIV can be avoided by ABC (abstinence, partner reduction, condom use) Number of male casual partners past month Number of commercial male partners past month Number of transgender past partners month Number of casual female partners past month Condom with casual female partner past month consistently in male-to-male anal sex in the previous month always used condoms with casual female partners were in comparison with MSM who never had sex with a female more likely to have used condoms consistently with male (OR = 0.39; 95% CI = 0.25–0.61, while MSM who partners as well (OR = 4.72; 95% CI = 2.26–9.84).
prevalence was measured for both groups [and asizeable multiple of that for the general population in Recent data and analyses indicate that MSM are at elevated risk for HIV infection in many low and middle income In the multivariate analyses, two factors had strong net countries ]. The 2007 IBBS data and the analyses associations with HIV-positive status: use of metham- undertaken in the present study confirm that that MSM in phetamines or similar drugs in the prior 3 months and Indonesia are indeed at elevated risk for HIV infection. A Chlamydia or gonorrhea infection at the time of the survey.
sizeable proportion (27%) of MSM reported having HIV-positive status was also associated with current rectal unprotected anal sex with multiple male partners, both Chlamydia or gonorrhea infection when the latter factor casual and commercial, in the month prior to the IBBS. The was the outcome variable. The observed reciprocal asso- levels of sexual risk-taking that may be deduced from the ciation between HIV and rectal STIs derives from their self-reported behavioral data are confirmed by quite high being transmitted through similar sexual behaviors. How- levels of rectal STIs. Roughly 32% tested positive for ever, rectal Chlamydia and gonorrhea also increases both either rectal Chlamydia or gonorrhea, while 6.3% tested the risk of HIV transmission by increasing HIV shedding positive for either urethral Chlamydia or gonorrhea. The and susceptibility to HIV infection by disrupting mucosal latter figure is comparable to the prevalence observed among a sample of 3,000 men in ‘‘high-risk’’ occupational Recent literature points to the use of methamphetamines groups in the 2007 IBBS, who presumably became infected and similar psychostimulants as a risk factor for HIV via unprotected sex with female sex workers ]. The infection among MSM –The use of methampheta- observed prevalence of syphilis, 3.2%, was slightly higher mines and similar psycho-stimulants was associated with a than that measured for a sample of Jakarta MSM in 2002 44% reduction in the odds of having used condoms con- sistently during anal sex with male partners in the month The data also confirm that the sexual networks of prior to the survey, a relationship that has also been Indonesian MSM are diverse, as they are in much of Asia observed in other studies. Methamphetamine use is also [, In addition to many MSM having multiple male known to be associated with prolonged and rough anal sex partners, 41% of MSM had had sex with a female partner in ], which when combined with reduced condom use, the year prior to the survey, and 27% in the prior month would appear to be a fairly dangerous combination. While alone. The bisexuality of many MSM in Indonesia holds only about 15% of MSM in the cities studied reported use the potential for HIV spread through risky male-male sex of such drugs in the prior 3 months, use was much higher to be further spread into heterosexual networks (and vice in Batam, Riau Islands (30.7%) and Jakarta (25.0%), and versa), particularly given the observed lower level of there is anecdotal evidence that the use of methampheta- condom use with female partners, thus potentially con- mines is growing in Indonesia among both MSM and tributing to a wider HIV/AIDS epidemic in the country.
injecting drug users. The explanation for higher use in However, bisexuals had lower odds of having a rectal STI Batam, which is only a one-hour ferry ride from Singapore, than exclusive homosexual MSM, which likely reflects the and Jakarta likely involves some combination of higher absence of risk of rectal STIs associated with vaginal sex disposable incomes, greater access to drugs, and greater with women; that is, men whose sexual encounters in the contact with international visitors.
prior month were spread among males and females reduced Increasing consistent condom use is pivotal for HIV their number of exposures to rectal STIs via reduced fre- prevention for MSM in Indonesia. Here, the study findings quency of anal sex. Moreover, bisexual men were less are instructive. On the positive side, the findings suggest likely to practice exclusively receptive anal sex with other that further increasing HIV/AIDS-related awareness and knowledge among MSM should lead to increases in con- With regard to HIV prevalence, the 8.0% prevalence sistent condom use. The positive association between observed among MSM in Jakarta in 2007 is substantially having recently been tested for HIV and increased likeli- higher than that observed in 2002—3.6% among male sex hood of consistent condom use is also promising insofar as workers and 2.5% among other MSM Prevalence both HIV counseling and testing service availability and levels in the two other cities in which HIV prevalence was service use by MSM have been increasing rapidly in measured in the 2007 IBBS, Bandung (West Java) and Indonesia in recent years. However, while the observed Surabaya (East Java) appear, however, to be somewhat association might indicate that having recently learned lower (2.0 and 5.6%, respectively). To put this in per- one’s HIV status is associated with the adoption of pro- spective, these data indicate that MSM have HIV preva- tective behaviors, it is also possible that men who were lence rates that are comparable to those of ‘‘indirect’’ sufficiently well informed and motivated to get tested for female sex workers both in the three cities for which HIV HIV are also more likely to use condoms. In the event that the relationship is causal as opposed to spurious, the small transmission and prevention measures. Future HIV/AIDS number of men tested for HIV more than a year prior to the prevention efforts must focus on motivating MSM to use survey is unfortunately insufficient to support inferences as condoms more consistently in all sexual relationships.
to whether the effect of HIV testing on safer sex behavior is Addressing drug use among MSM should also be assigned short-term in nature or is likely to be sustained over a a high priority in future prevention efforts.
The findings that (a) consistency of condom use by Primary financial support for this research was provided by the US Agency for International Development (USAID) MSM does not vary across male partner types and (b) and the Indonesian Partnership Fund.
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