AIDS Behav DOI 10.

1007/s10461-009-9590-6

ORIGINAL PAPER

Sexual Risk Taking, STI and HIV Prevalence Among Men Who Have Sex with Men in Six Indonesian Cities
Guy Morineau Naning Nugrahini Pandu Riono Nurhayati Philippe Girault Dyah Erti Mustikawati Robert Magnani

Springer Science+Business Media, LLC 2009

Abstract Using surveillance data on men who have sex with men (MSM) from six Indonesian cities, this article reports prevalence of sexual risk taking, HIV and other sexually transmitted infections. Factors associated with HIV, other STIs and consistent condom use were assessed. Behavioral data were collected from 1,450 MSM, among whom 749 were tested for HIV and syphilis and 738 for gonorrhea and Chlamydia. Associations were assessed using multivariate logistic regression. Over 80% of MSM knew HIV transmission routes, 65% of MSM had multiple male sexual partners, 27% unprotected anal sex with multiple male partners, and 27% sex with a female in the prior month. Consistent condom use ranged from 30 to 40% with male partners and 20 to 30% with female partners, depending upon partner type. HIV prevalence averaged 5.2%, but was 8.0% in Jakarta. Prevalence of rectal gonorrhea or Chlamydia was 32%. Multivariate analyses revealed recent methamphetamine use and current rectal gonorrheal or chlamydial infection to be associated with HIV infection. The data conrm diverse sexual networks and substantial sexual risk-taking, despite relatively high levels of education and HIV-related knowledge. In addition to promoting partner reduction and more consistent

condom and lubricant use, prevention efforts must also address substance abuse. Keywords HIV/AIDS STI Risk behaviors Men who have sex with men, Indonesia

Introduction With the exception of Papua and West Papua Provinces on the island of New Guinea, where a low-prevalence generalized HIV/AIDS epidemic has emerged (population prevalence = 2.4%), HIV/AIDS in Indonesia remains concentrated in certain most-at-risk-groups [13]. While the HIV/AIDS epidemic in Indonesia has been driven primarily by the sharing of contaminated drug injecting equipment since the late 1990s, it is currently believed that the role of injecting drug use in driving HIV/AIDS may be peaking or have already peaked [2, 3]. Indeed, the Indonesian National AIDS Commission projects that between 2007 and 2027 men who are infected via unprotected sex with female sex workers and with other men will account for the majority of new HIV infections [3]. These projections are consistent with those of the Commission on AIDS in Asia for the region as a whole [2]. Responding to an expanding HIV/AIDS epidemic among men who have sex with men (MSM) presents a 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 difcult to reach with information and services in a systematic way. This is compounded by a limited evidence base concerning numbers of MSM, their risk-taking and health-seeking behaviors, and infection rates. Aside from limited behavioral

G. Morineau (&) P. Girault Family Health International, Asia/Pacic Regional Ofce, 19th Floor, Sindhorn Building, Tower 3, 130 -132 Wireless Rd, Lumpini, Bangkok 10330, Thailand e-mail: gmorineau@fhi.org N. Nugrahini D. E. Mustikawati Sub-Directorate for HIV/AIDS & STIs, Ministry of Health, Republic of Indonesia, Jakarta, Indonesia P. Riono Nurhayati R. Magnani Family Health International, Jakarta, Indonesia

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questions for small samples of MSM included in behavioral surveillance surveys conducted in 20022003 [4] and 20042005 [5], the only other available behavioral data come from qualitative studies with uncertain generalizability [6, 7]. Biological data (i.e., HIV and STI prevalence rates) are yet scarcer. Transgenders (i.e., Waria) in Jakarta were included in Ministry of Health sentinel surveillance through 2005, and the MOH undertook a small study of MSM in which HIV and syphilis prevalence was measured for a sample of 750 MSM in Jakarta [8, 9], but surveillance otherwise has not covered MSM. The Ministry of Health estimated that there were about 767,000 MSM in the country as of 2006 (range 385,0001,150,000) [10]. This paper takes advantage of biological and behavioral surveillance data gathered from MSM in six Indonesian cities in the 2007 Integrated Biological-Behavioral Surveillance (IBBS) surveys to assess the current epidemiologic situation among MSM and determine factors associated with HIV and other STI infection. The IBBS represent the rst large-scale, systematic data collection in Indonesia for this important sub-population with both behavioral and biological data. These data are timely in that if, as has been suggested by the projections cited above, HIV/AIDS in Indonesia is evolving such that sexual transmission among MSM will play a more signicant role in future transmission, it is crucial that national health authorities understand the current realities so that appropriate action can be taken.

groups and local health authorities. Survey subjects were selected via two-stage, time-location sampling (TLS). At the rst stage, locations were randomly selected with probability proportional to the estimated number of men at each location. A sample of MSM of size proportional to venue size was then selected via systematic-random sampling. All selected MSM were asked to voluntarily participate in a behavioral survey using a structured questionnaire, and in Jakarta and Surabaya provide biological samples. In Batam, Bandung, and Malang, MSM were recruited through respondent driven sampling (RDS). Eight MSM seeds were recruited purposively in each city, ensuring that they (1) lived in the city, (2) were aged 1549, and (3) were part of an extended network of MSM. All seeds and subsequent recruits were each given three (3) coupons to recruit other MSM they knew. Recruiters received US$ 4 for each successful recruit. The survey was terminated when the target sample size was reached in each city. Recruits in Bandung were asked to provide biological samples. The use of different sampling methods was part of the process of developing a surveillance system for MSM. In the 2007 IBBS, RDS was tried as an alternative to TLS in the smaller cities to assess its advantages in reaching more hidden MSM. The results will be used to assess and guide choice of sampling methods for MSM in future rounds of surveillance. Field Data Collection

Methods Sampling Behavioral survey data were collected from independent samples of 1,450 MSM in six Indonesian cities between August and November 2007. The cities included Bandung (West Java), Jakarta, Malang (East Java), Medan (North Sumatra), Semarang (Central Java) and Surabaya (East Java). MSM interviewed in Bandung, Jakarta and Surabaya were asked to provide biological samples, and 749 men were successfully tested for HIV, syphilis, and urethral Chlamydia and gonorrhea, and 738 for rectal Chlamydia and gonorrhea. MSM were dened as men who have sex with other men either for commercial gain or as a matter of sexual preference. Data were also obtained from independent samples of transgenders, but as the underlying dynamics of the HIV/AIDS epidemic among transgenders differ markedly from MSM as dened above, they are not considered in this article. In Jakarta, Surabaya, and Medan, sampling frames were developed from mappings of locations where MSM could be found. These were produced jointly by non-governmental organizations (NGOs) providing services to such Survey eld teams were drawn from staff of provincial ofces of the Central Statistics Bureau, provincial health departments, and CBOs and NGOs serving MSM in the survey area. Survey staff received specialized training on survey eld procedures. In as private a location as could be found, interviewers explained the study procedures, sought informed consent and gathered behavioral survey data using structured, pre-coded questionnaires. A nurse collected blood through nger prick, and participants provided self-collected rectal swabs and rst-void urine. Behavioral and biological data were gathered anonymously and were linked via special ID numbers. Participants received a coupon for free HIV counseling and testing at a nearby Community Health Center and were given their participant number in order to access their STI test results and receive treatment free of charge if needed. Laboratory methods. Blood specimens were collected in EDTA tubes, stored at 46C and transported to a government provincial laboratories within ve hours to be tested for HIV and syphilis. HIV was tested using two rapid tests conducted in parallel: SD Bioline HIV 1/2 3.0 (Standard Diagnostic, Korea, South Korea) and Determine HIV-1 (Abbott, Abbott Park, IL). Discrepant results were re-tested at the

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National Reference Laboratory using two ELISA: Murex HIV 1.2.0 (Murex Biotech, Dartford, UK) and Vironostika HIV-1 Plus O (Biomerieux, Marcy lEtoile, France) and results that remained discordant were classied as indeterminate. Syphilis was tested using a treponemal test: Determine Syphilis TP (Inverness Medical, Bedford, UK). Rectal swabs and urine specimens were tested for Chlamydia and gonorrhea via PCR using Cobas Amplicor (Roche, Basel, Switzerland). Data Analysis Behavioral data were double entered using CSPro 2.6.007 (US Census Bureau). Laboratory data were entered using Microsoft Excel. Analysis was performed using Stata 9.0 (Stata Corporation, College Station, TX). The implications of use of two different sampling methods were assessed by comparing background characteristics of respondents by type of sampling methodology. Subsequent analysis was performed on multisite pooled data, assuming a stratied simple random sampling design. Simple logistic regression was used to assess associations of background characteristics and risk behaviors with three separate outcomes: HIV, rectal infection with Chlamydia or gonorrhea, and consistent condom use in anal sex with male partners in the past month. Differences were assessed using the Wald test, and P values of \ 0.05 were considered signicant. Multivariate logistic regression was used to determine the net contributions of factors that were signicant at the P B .20 level or better in bivariate analyses. Factors were eliminated in a backward stepwise elimination process based upon their contribution to variance explained until only factors signicant at the P \ .05 level remained in the nal models.

held salaried position at the time of the survey, with another 26% being independent workers/performing odd jobs. Nine percent worked in a salon/beauty parlor, which often serve as men to men sex trade locations. Only 11% of MSM had resided in the city in which they were interviewed for 1 year or less, whereas 58% had lived in their current city of residence for 10 years or more and 41% their whole life. As shown in Table 1, differences in background characteristics of MSM sampled via TLS were signicantly different (P \ .05) from those sampled via RDS on ve of the six characteristics considered. However, although statistically signicant, the differences are not pronounced enough to preclude combining the two samples. Furthermore, the only background characteristic on which there was not a signicant difference depending upon sampling method, level of education, was the only characteristic found to be signicantly associated with any of the outcome variables in multivariable analyses. Consequently, all analyses were undertaken with the full sample of MSM. Knowledge of HIV/AIDS-related Risk and Protective Factors MSM included in the IBBS were knowledgeable about HIV/AIDS (data not shown). Knowledge questions that were correctly answered by over 80% of MSM included: protection offered by condoms from transmission of HIV during vaginal and anal sex; HIV transmissibility via sharing of contaminated drug injecting equipment, during the course of child birth, and through breastfeeding infants; and that it was not possible to recognize HIV-infected persons by their appearance. However, 41% thought HIV transmission could be prevented by taking antibiotics before having sex and 27% believed that HIV could be transmitted through sharing food utensils. Sexual Activity and Other Risk-taking Behaviors

Results Background Characteristics Respondent background data are displayed in Table 1 separately for MSM sampled via time-location sampling (TLS) versus respondent-driven sampling (RDS). In the aggregate, respondents averaged just over 28 years of age. Although most MSM were never married (to a female), 15% were currently and another 5% were formerly married. The most common living arrangement was with family (i.e., parents and/or siblings; 44%), with another 26% living alone and 19% living with friends. Six percent lived with a regular female partner and 5% a regular male partner. Education levels were relatively high, with 58% of respondents having attended senior high school and another 24% college/university. A large proportion of MSM (45%) The initial sex partner of most MSM (66%) was another male, although 32% reported rst sex with a female and 2% with a transgender (not shown). Mean age at rst sex was 18.2 years (Table 2). Nearly 63% of MSM had ever bought or sold sex, with a mean duration of almost 7 years since rst commercial sex. Ten percent reported ever having been forced into sex. Fifty-seven percent of men reported having a regular sex partner at the time of the survey interview, two-thirds of whom were male. The data on sexual partners in the year prior to the survey indicate both volume and diversity. Most MSM had sex with a casual male partner in the prior year and over one-half with a regular male partner; that is, a partner in a long-term relationship as dened by the respondent. Selling

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AIDS Behav Table 1 Background characteristics of MSM in six Indonesian cities

TLS* n = 750 Age Mean Median Age group 1524 2539 C35 Education BJunior high school Senior high school College/university Live with Alone Friends Family/siblings Wife/female regular partner Regular male partner Main source of income Salaried position Independent/odd jobs Work in salon/beauty parlor Student Other Duration of residence in current city B1 year 25 years 69 years 1038 years Whole life 13.0 28.6 9.3 16.3 42.1 50.9 21.0 11.8 3.0 13.3 29.0 19.2 41.4 7.1 3.2 15.9 59.5 24.6 33.3 44.4 22.3 28.8 27.0

RDS** n = 700

P value

Total

27.5 26.0 42.7 37.7 19.6 19.3 57.1 23.6 23.4 18.0 46.9 5.1 6.6 38.9 30.3 5.9 10.6 14.4 8.2 34.4 11.5 17.6 39.8

0.001

28.2 27.0

0.001

37.9 41.2 21.0

0.235

17.6 58.3 24.1

0.001

26.3 18.6 44.0 6.2 4.9

\0.001

45.1 25.5 8.9 6.7 13.9

0.013

10.7 31.4 10.3 16.9 41.0

* Time location sampling ** Respondent driven sampling

sex to other MSM was more common than buying sex from MSM. A sizeable proportion of respondents also had sex with females during the reference yearmost often with casual female partners, but 14% also sold sex to and 10% bought sex from females during the previous year. Sexual partners in the month prior to the survey were also diverse, but were dominated by casual male partners, male clients and casual female partners. Seventy-ve percent of MSM had sex with a casual male partner in the prior month, with a mean of 2.8 partners. Thirty-ve percent of MSM sold sex to a male client in the previous month with a mean of 6.6 clients (median = 3.0), while 13% reported buying sex from another male. Twenty-six percent of MSM had sex with a casual female partner in the past month. Approximately 15% of MSM reported using methamphetamine before having sex, in the 3 months prior to the survey. However, methamphetamine use was much higher in two citiesJakarta (31%) and Medan, North Sumatra (25%; data not shown).

Nearly 35% of MSM had received an STI check-up at a clinic in the 3 months prior to the survey, reecting recent efforts in Indonesia to promote routine check-ups among sexually active MSM. Approximately 25% of respondents reported having had STI symptoms in the prior year. Of those, less than half received professional medical treatment, more often from privatethan public-sector service providers. A plurality of MSM (36%) either self-treated or sought traditional treatment, while 20% of cases went untreated. About 40% of men had ever been tested for HIV, the large majority in the previous year, again likely reecting recent expansion of HIV/AIDS program coverage for MSM in Indonesia. Condom Use Condom use at last anal sex with male partner exceeded 60%, but was substantially lower at last vaginal sex with female partners (Table 3). With female partners, condom use was more common with commercial than with casual partners,

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AIDS Behav Table 2 Risk-taking and health-seeking behaviors among MSM n Age at rst sex Mean Median Ever had commercial sex (%) Number of years since rst sold sex Mean Median Gender of permanent partner (%) No permanent partner Man Woman Transgender Type of partners past year (%) No partner Male regular partner Male casual partners Male clients Male sex workers Transgenders Female casual partners Female sex workers Female clients Type of partners past month (%) No partner Male partners only Female partners only Both male and female Male casual partners Male clients Male sex workers Transgenders Female casual partners Female sex workers Female clients 315 743 44 348 1,066 438 179 112 349 63 103 21.7 51.2 3.0 24.0 75.4 34.7 12.5 9.0 26.3 5.0 8.4 11 806 1,256 619 283 194 525 125 173 0.8 56.8 86.7 47.2 19.7 15.7 40.4 9.9 14.0 613 555 225 22 43.3 39.2 15.9 1.6 909 6.9 5 909 1,405 18.2 18.0 62.7 Values Table 2 continued n Values

Heath seeking behaviors at last symptomatic episode of STI (%) No treatment Self treatment Private doctor/nurse Public hospital/community health center When had last HIV test (%) Never tested Tested in the past year Tested more than a year ago 782 446 77 59.9 34.2 5.9 70 128 91 67 19.7 36.0 25.6 18.8

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 condomsbetween 26 and 34% with male commercial and casual male partners, and only 12% with transgender partners. 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 depending upon 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 sex66% (data not shown). HIV and STI Prevalence Data on HIV and other STI prevalence for MSM in three cities are displayed in Table 4. HIV prevalence for the full 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 Chlamydia or gonorrhea. Prevalence of rectal STIs was considerably higherChlamydia 21%, gonorrhea 19%, and either of the two infections 32%. Factors Associated with HIV, Other STIs and Consistent Condom Use The results of multiple logistic regression analyses undertaken to identify factors associated with HIV-positive

Mean number of partners past month (among those who had this type of partner) Male casual partners Male clients Male sex workers Transgenders Female casual partners Female sex workers Female clients Ever forced into sex (%) Used methamphetamines before sex in past 3 months (%) Had routine STI check-up in past 3 months (%) Had STI symptoms in the past year (%) 1,066 438 179 112 349 63 103 74 211 927 353 2.8 6.6 1.5 1.1 1.5 1.7 2.8 10.1 14.6 34.7 24.5

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AIDS Behav Table 3 Use of condom and lubricant by type of sexual partners Male casual Male client Male sex Waria partner (n) % (n) % worker (n) % (n) % Used condom at last sex Past month Always used condom Always used lubricant Never used condom and lubricant NA not available (information not collected) (286) 31.7 (266) 29.5 (128) 14.2 (134) 33.3 (138) 34.2 (104) 25.8 (25) 15.2 (51) 30.7 (42) 25.5 (35) 21.2 (53) 13.2 (9) 36.0 (40) 12.1 (9) 15.3 (21) 19.8 NA NA NA NA NA NA (3) 12.0 NA (3) 12.0 NA (4) 16.0 NA (713) 61.9 (380) 66.4 (179) 62.4 Female casual FSW partner (n) % (n) % Female client (n) %

(108) 60.7 (178) 32.5

(63) 41.7 (95) 49.5

Always used both condom and lubricant (214) 23.8

Table 4 Prevalence of HIV and other sexually transmitted infections (STI) among MSM Pathogens and localization City Jakarta n HIV Syphilis Urethral chlamydia Urethral gonorrhea Urethral chlamydia or gonorrhea Rectal chlamydia Rectal gonorrhea Rectal chlamydia or gonorrhea 248 249 250 250 250 242 242 242 % (95% CI) 8.1 (5.112.6) 3.2 (1.56.6) 6.8 (4.011.4) 2.0 (0.94.6) 8.4 (5.313.2) 21.9 (17.027.8) 18.6 (14.523.5) 32.2 (26.338.8) Bandung n 249 250 249 249 249 246 247 247 % (95% CI) 2.0 (0.84.7) 5.6 (3.39.3) 3.6 (1.96.8) 2.4 (1.15.3) 5.2 (3.08.8) 19.5 (15.025.0) 22.3 (17.527.9) 33.6 (28.939.8) Surabaya n 250 250 250 250 250 249 249 249 % (95% CI) 5.6 (3.39.3) 4.0 (2.27.3) 4.4 (2.47.8) 1.2 (0.43.7) 5.2 (3.08.8) 21.3 (16.626.8) 14.9 (11.019.9) 29.3 (24.035.3) All cities n 747 749 749 749 749 737 738 738 % (95% CI) 5.2 (3.87.2) 4.3 (3.06.0) 4.9 (3.56.9) 1.9 (1.13.1) 6.3 (4.78.4) 20.9 (18.124.0) 18.6 (16.021.4) 31.7 (28.435.2)

status, presence of other STI infections, and consistent condom use in male-to-male anal sex in the prior month, respectively, are presented in Tables 5, 6 and 7. With regard to the results with HIV status as the outcome variable, although a number of factors were associated with HIV-positive status at the bivariate level, only two variables retained signicant associations in the multivariate analyses(1) use of methamphetamines or similar drugs in the prior 3 months (OR = 2.69; 95% CI = 1.335.43) and (2) Chlamydia or gonorrhea infection at the time of the survey (OR = 2.04; 95% CI = 1.063.92; Table 5). After accounting for the effects of other factors, four factors were associated with Chlamydia or gonorrhea infection at the time of the survey(1) forced into sex in the prior year (OR = 2.21; 95% CI = 1.393.50), (2) number of casual male partners in the prior month (OR = 1.08; 95% CI = 1.031.12), (3) HIV infection(OR = 2.41; 95% CI = 1.204.84), and (4) having had sex with a female partner in the past year (OR = 0.54; 95% CI = 0.380.77; Table 6). Seven factors were found to be associated with consistent condom use in anal sex in the prior month in the multivariable analyses (Table 7). Increasing levels of

education were associated with increasingly higher likelihood of consistent condom use. MSM who attended senior high school were more likely to have used condoms consistently than those with junior high level or below levels of education (OR = 1.67; 95% CI = 1.082.58), and MSM who attended college/university being more than twice as likely (OR = 2.16; 95% CI = 1.333.52). Other factors associated with higher likelihood of consistent condom use included having sufcient knowledge of HIV transmission and prevention to protect themselves (OR = 1.41; 95% CI = 1.041.88) and having been tested for HIV in the past year (OR = 2.25; 95% CI = 1.66 3.04). Several factors were associated with reduced likelihood of consistent condom use. The data indicate that consistent condom use during anal sex declines with increased duration of selling sex, with MSM who had been selling sex 24 years being 43% less likely to use condoms than men who never sold sex, while those who sold sex for 5 years or more were 45% less likely to have used condoms consistently. MSM who had sold sex for 1 year or less did not, however, differ signicantly with regard to consistent condom from men who had never sold sex. Use of

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AIDS Behav Table 5 Risk factors associated with HIV infection

Age group 1524 2534 C35 Education BJunior high school Senior high school College/University Know ABC No Yes Age at rst sex Duration since rst selling sex Never sold sex B1 year 24 years C5 years Ever forced into sex past year No Yes Sex with female casual partner past year No Yes Sex with transgender past year No Yes 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 Not always Always Use of lubricants in anal sex in last month Not always Always Used methamphetamine in last 3 months No Yes Currently infected with rectal CT or NG No Yes Currently infected with syphilis No Yes Currently infected with urethral CT or NG No * P \ .05, ** P \ .01 Yes 1 0.39 (0.052.90) 1 1.95 (0.576.71) 1 2.13* (1.114.06) 1 2.04* (1.063.92) 1 2.77** (1.385.56) 1 2.69** (1.335.43) 1 0.81 (0.361.81) 1 0.42 (0.053.34) 1 1.71 1.06 1.04* 1.01 0.99 0.69 (0.714.22) (1.001.12) (1.011.07) (0.831.25) (0.841.18) (0.222.17) 1 1.41 (0.732.70) 1 0.36 (0.081.51) 1 0.56 0.84 0.59 (0.074.34) (0.391.79) (0.251.43) 1 1.62 1.02 (0.843.09) (0.941.10) 1 1.87 1.39 (0.714.97) (0.444.33) 1 1.8 0.83 (0.883.66) (0.292.38)

Bivariable OR (95% CI)

Multivariable OR (95% CI)

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AIDS Behav Table 6 Risk factors associated with rectal infection with chlamydia or gonorrhea Age group 1524 2534 C35 Education BJunior high school Senior high school College/University Duration since rst selling sex Never sold sex B1 year 24 years C5 years Ever forced into sex past year No Yes Sex with casual female partner past year No Yes Sex with transgender past year No Yes 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 No casual male partner Inconsistent condom use Always used condom Always used lubricant with casual male past month Always used of lubricant in anal sex past month Condom use casual female partner past month No casual female partner Inconsistent condom use Always used condom Used methamphetamine in last 3 months No Yes Currently infected with HIV No Yes * P \ .05, ** P \ .01 1 2.13* (1.114.06) 1 2.41** (1.204.84) 1 1.33 (0.882.00) 1 0.65* 1.12 (0.440.98) (0.462.72) 1 1.04 1.07** 1.01 1.05 1.08 1 1.22 1.26 0.96 0.80 (0.851.74) (0.791.99) (0.831.11) (0.531.19) (0.621.74) (1.021.12) (0.991.03) (0.941.17) (0.991.18) 1.08** (1.031.12) 1 0.62** (0.440.86) 1 0.54** (0.380.77) 1 1.96** (1.263.05) 1 2.21** (1.393.50) 1 1.42 0.92 0.61* (0.653.12) (0.631.33) (0.410.92) 1 1.22 1.13 (0.811.84) (0.701.84) 1 1.02* 0.58 (0.731.44) (0.370.92)

Bivariable OR (95% CI)

Multivariable OR (95% CI,)

methamphetamines, ecstasy or similar psychostimulants in the prior 3 months was associated with signicantly lower likelihood of consistent condom use (OR = 0.59; 95% CI = 0.370.94).

The nal factor associated with reduced odds of consistent condom use was condom use with female partners. MSM who did not used condoms consistently with casual female partners were also less likely to have used condoms

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AIDS Behav Table 7 Risk factors associated with consistent condom use in anal sex past month Age group 1524 2534 C35 Education BJunior high school Senior high school College/University No Yes Duration since rst selling sex Never sold sex B1 year 24 years C5 years Sex with transgender past year No Yes Had sex with women past year No Yes Sex with female casual past year No Yes 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 Number of commercial female past month Had sex with women past month No Yes Condom with casual female partner past month No female casual partner Not always Always Used methamphetamine in last 3 months No Yes Tested for HIV Never tested Tested past year * P \ .05, ** P \ .01 Tested before last year 1 2.05** 1.23 (1.542.73) (0.642.36) 1 2.25** 1.54 (1.663.04) (0.773.06) 1 0.54** (0.350.83) 1 0.59* (0.370.94) 1 0.36** 3.69** (0.240.56) (1.837.43) 1 0.39** 4.72** (0.250.61) (2.269.84) 1 0.51** (0.370.72) 1 0.53** 1.01 1.00 1.13 0.66** 0.95 (0.390.73) (0.971.04) (0.981.02) (0.911.39) (0.510.86) (0.851.07) 1 0.51** (0.380.69) 1 0.13** (0.070.25) 1 1.79** 2.59** 1 1.43* 1 0.59 0.51** 0.57** (0.261.35) (0.360.72) (0.410.79) (1.091.89) (1.182.71) (1.634.12) 1 1.67* 2.16** 1 1.41* 1 0.85 0.57** 0.55** (0.352.03) (0.390.83) (0.390.78) (1.041.88) (1.082.58) (1.333.52) 1 1.14 1.33 (0.841.55) (0.921.92)

Bivariable OR (95% CI)

Multivariable OR (95% CI)

Know that HIV can be avoided by ABC (abstinence, partner reduction, condom use)

consistently in male-to-male anal sex in the previous month in comparison with MSM who never had sex with a female (OR = 0.39; 95% CI = 0.250.61, while MSM who

always used condoms with casual female partners were more likely to have used condoms consistently with male partners as well (OR = 4.72; 95% CI = 2.269.84).

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Discussion Recent data and analyses indicate that MSM are at elevated risk for HIV infection in many low and middle income countries [2, 11]. The 2007 IBBS data and the analyses undertaken in the present study conrm that that MSM in Indonesia are indeed at elevated risk for HIV infection. A sizeable proportion (27%) of MSM reported having unprotected anal sex with multiple male partners, both casual and commercial, in the month prior to the IBBS. The levels of sexual risk-taking that may be deduced from the self-reported behavioral data are conrmed by quite high levels of rectal STIs. Roughly 32% tested positive for either rectal Chlamydia or gonorrhea, while 6.3% tested positive for either urethral Chlamydia or gonorrhea. The latter gure is comparable to the prevalence observed among a sample of 3,000 men in high-risk occupational groups in the 2007 IBBS, who presumably became infected via unprotected sex with female sex workers [12]. The observed prevalence of syphilis, 3.2%, was slightly higher than that measured for a sample of Jakarta MSM in 2002 (1.7%) [8, 9]. The data also conrm that the sexual networks of Indonesian MSM are diverse, as they are in much of Asia [6, 7, 13]. In addition to many MSM having multiple male partners, 41% of MSM had had sex with a female partner in the year prior to the survey, and 27% in the prior month alone. The bisexuality of many MSM in Indonesia holds the potential for HIV spread through risky male-male sex to be further spread into heterosexual networks (and vice versa), particularly given the observed lower level of condom use with female partners, thus potentially contributing to a wider HIV/AIDS epidemic in the country. However, bisexuals had lower odds of having a rectal STI than exclusive homosexual MSM, which likely reects the absence of risk of rectal STIs associated with vaginal sex with women; that is, men whose sexual encounters in the prior month were spread among males and females reduced their number of exposures to rectal STIs via reduced frequency of anal sex. Moreover, bisexual men were less likely to practice exclusively receptive anal sex with other males (2.5 vs. 11.2%, P \ 0.001). With regard to HIV prevalence, the 8.0% prevalence observed among MSM in Jakarta in 2007 is substantially higher than that observed in 20023.6% among male sex workers and 2.5% among other MSM [8, 9]. Prevalence levels in the two other cities in which HIV prevalence was measured in the 2007 IBBS, Bandung (West Java) and Surabaya (East Java) appear, however, to be somewhat lower (2.0 and 5.6%, respectively). To put this in perspective, these data indicate that MSM have HIV prevalence rates that are comparable to those of indirect female sex workers both in the three cities for which HIV

prevalence was measured for both groups [14], and a sizeable multiple of that for the general population in Indonesia. In the multivariate analyses, two factors had strong net associations with HIV-positive status: use of methamphetamines or similar drugs in the prior 3 months and Chlamydia or gonorrhea infection at the time of the survey. HIV-positive status was also associated with current rectal Chlamydia or gonorrhea infection when the latter factor was the outcome variable. The observed reciprocal association between HIV and rectal STIs derives from their being transmitted through similar sexual behaviors. However, rectal Chlamydia and gonorrhea also increases both the risk of HIV transmission by increasing HIV shedding and susceptibility to HIV infection by disrupting mucosal barriers [15, 16]. Recent literature points to the use of methamphetamines and similar psychostimulants as a risk factor for HIV infection among MSM [1722]. The use of methamphetamines and similar psycho-stimulants was associated with a 44% reduction in the odds of having used condoms consistently during anal sex with male partners in the month prior to the survey, a relationship that has also been observed in other studies. Methamphetamine use is also known to be associated with prolonged and rough anal sex [23], which when combined with reduced condom use, would appear to be a fairly dangerous combination. While only about 15% of MSM in the cities studied reported use of such drugs in the prior 3 months, use was much higher in Batam, Riau Islands (30.7%) and Jakarta (25.0%), and there is anecdotal evidence that the use of methamphetamines is growing in Indonesia among both MSM and injecting drug users. The explanation for higher use in Batam, which is only a one-hour ferry ride from Singapore, and Jakarta likely involves some combination of higher disposable incomes, greater access to drugs, and greater contact with international visitors. Increasing consistent condom use is pivotal for HIV prevention for MSM in Indonesia. Here, the study ndings are instructive. On the positive side, the ndings suggest that further increasing HIV/AIDS-related awareness and knowledge among MSM should lead to increases in consistent condom use. The positive association between having recently been tested for HIV and increased likelihood of consistent condom use is also promising insofar as both HIV counseling and testing service availability and service use by MSM have been increasing rapidly in Indonesia in recent years. However, while the observed association might indicate that having recently learned ones HIV status is associated with the adoption of protective behaviors, it is also possible that men who were sufciently well informed and motivated to get tested for HIV are also more likely to use condoms. In the event that

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the relationship is causal as opposed to spurious, the small number of men tested for HIV more than a year prior to the survey is unfortunately insufcient to support inferences as to whether the effect of HIV testing on safer sex behavior is short-term in nature or is likely to be sustained over a longer period of time. The ndings that (a) consistency of condom use by MSM does not vary across male partner types and (b) condom use with female partners was associated with higher condom use in anal sex with male partners suggest that Indonesian MSM tend to use condoms, or not, without regard to partner type (although the correlation is not perfect as condom use with female partners was less frequent than with male partners). Condom promotion efforts should thus focus on increasing condom use with all partners as attempting to differentiate between more and less risky partners might unnecessarily complicate behavior change communication messages. However, it should be noted that most interventions that target MSM have been developed for gay self-identied MSM whose sex partners are predominantly other men. However, MSM who have both male and female partners, in the case of Indonesia including married men who sell sex to other males as a primary or additional source of income, may not be reached by or respond to such interventions. In Indonesia, locations where male sex workers work are fairly well established, and it may be feasible to use different strategies and messages. In other settings, it may be necessary to just target men with a full range of risk reduction messages that address both vaginal and anal sex. Finally, the observed association of having experienced forced sex with higher likelihood of current gonorrhea or chlamydial infection merits attention. While to some extent this association might be the result of infection acquired during recent episodes of forced sex, it also raises the issue of the psychological consequences of rape as a risk factor for subsequent behavior. Indeed, recent literature points to associations between history of rape and higher prevalence of drug use, selling sex and unprotected sex [24, 25]. This would suggest that counseling and support services to address forced sex among MSM might be needed as part of service packages for MSM. At present, HIV prevalence rates are not as high among MSM in Indonesia as in other Asian countries [11, 26]. However, the continued high prevalence of unprotected anal sex with multiple concurrent male partners, the existence of a signicant and apparently growing pool of HIV infection within male sexual networks, and signicant levels of sexual contact with females constitute ideal conditions for accelerating the spread of HIV both within the ranks of MSM and to the general population. MSM in Indonesia are relatively highly educated and appear to have a high level of awareness of basic facts on HIV

transmission and prevention measures. Future HIV/AIDS prevention efforts must focus on motivating MSM to use condoms more consistently in all sexual relationships. Addressing drug use among MSM should also be assigned a high priority in future prevention efforts.
Acknowledgments Primary nancial support for this research was provided by the US Agency for International Development (USAID) and the Indonesian Partnership Fund.

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