High HIV, hepatitis C and sexual risks among drug-using men who have sex with men in northern Thailand

Background: Men who have sex with men (MSM) and who use drugs have shown high HIV risks in Europe, and the Americas. We investigated MSM-drug user demographics, HIV sexual and drug use risks and behaviors in Chiang Mai, northern Thailand to identify prevention targets.

Methods: A total of 2005 males aged 13 years and older were enrolled during inpatient drug treatment from 1999-2000 and assessed for HIV, hepatitis C virus (HCV), syphilis, and for demographics and risks by questionnaire. Data were analyzed using χ² and multiple logistic regression to estimate odds ratios (ORs) and 95% confidence intervals (CIs).

Results: Of 2005 males in treatment, 1752 (87.4%) had ever had sex, and 66 of 1752 (3.8%) reported ever having sex with another man; mostly Katoey (transgendered male) partners. MSM had higher HIV rates (OR, 2.32; 95% CI, 1.36-3.96) and were younger (P = 0.002); more likely to be Thai (P < 0.0001); better educated (P < 0.0001); had more lifetime sex partners (P < 0.0001), more female partners (P = 0.002), more female paid partners (P < 0.0001), and been paid for sex (P < 0.0001). MSM were more likely to have ever injected (P < 0.0001), sold drugs, been in prison, injected in prison, used heroin, and to have HCV (OR, 2.59; 95% CI, 1.55-4.34).

Conclusions: Northern Thai MSM-drug users are at high HIV and HCV risk. In addition to sex risks with men, they have more sex with women and sex workers than other men, which fits Thai MSM patterns but not Western ones. Prevention must take into account their high rates of substance use and multiple partner types.

Introduction

Men who have sex with men and use and inject drugs (MSM-drug users) have shown high HIV prevalence and risks in Europe and the Americas ^[1-3]. The sexual and substance use behaviors of these men may be highly diverse. Non-injection drug use with cocaine and methamphetamine have been reported as risks for increased sexual exposures to HIV and sexually transmitted infections (STI) among MSM ^[4,5]. These HIV risks may be primarily mediated through increased sexual risk taking. Drug using men of diverse sexual orientations may sell or trade sex with other men for money or drugs ^[2,6-8]. Men engaged in these behaviors may also have heterosexual risks for HIV and STI, making risk attribution complex ^[3,7]. Finally, drug users are more likely to be incarcerated than other men ^[9], and studies have reported MSM sexual risks and risky drug use associated with incarceration ^[10]. Given the range of interactions of MSM and substance use risks, the prevention needs of these multiple risk men may differ.

Little is known about MSM behaviors and substance use in Asia. There is increasing recognition of the substantial role MSM behaviors have played in the HIV epidemics in Thailand, Indonesia, India, China, Pakistan, Vietnam, and other Asian settings where studies have been done ^[11-20]. This emerging body of research suggests a rich array of cultural expressions of MSM behavior, gender roles and definitions ^[11-13,21].

Thai culture classically has three genders: male, female, and Katoey ^[22]. Katoey are transgendered males who adopt female names, roles, and identities ^[22]. They are perceived as a second category of females: 'Puying Piset' or 'special women'. Men who have sex with Katoey are not generally perceived to be engaged in homosexual activity. Our group first encountered and investigated these Thai cultural norms in studies of HIV risks among Royal Thai Army conscripts ^[11]. We found that young northern Thai men who reported sex with other men or with Katoey, had elevated HIV and STI risks in comparison with men who reported only female partners (HM) ^[11]. They also had more female lifetime partners, were more likely to have used female sex workers, and alcohol and marijuana, than HM ^[11]. When asked if they had ever had sex 'with another man', 3.2% of these conscripts said yes. When this question was posed as 'with another man or with a Katoey', the response rate doubled to 6.5% of men, underscoring the need for culturally appropriate questioning.

Few studies have investigated MSM behaviors among populations of substance users in Thailand or elsewhere in Asia. In the Opiate Users Research (OUR) cohort we studied a population presenting for voluntary drug detoxification in northern Thailand ^[23]. We present here the results of analyses of the demographic characteristics of MSM drug users, their HIV, hepatitis C virus (HCV), and sexual and drug use risks and behaviors.

Methods

The methods for the OUR study have been presented in detail elsewhere ^[20]. Briefly, we enrolled 2005 substance-using males age 13 years and older at one inpatient drug treatment center during 1999-2000. Criteria included admission for treatment of opiate and/or methamphetamine use. Informed consent was obtained from all adults and from parents of participants under aged 18 years. The study was approved by the institutional review bodies of the Royal Thai Ministry of Public Health, the Research Institute for Health Sciences of Chiang Mai University, and the Johns Hopkins Bloomberg School of Public Health.

Interviews were conducted in 12 local languages. Instruments were developed using literature reviews, qualitative methods, and field tests. Participants admitted for opiate detoxification were treated with either a methadone taper protocol or tincture of opium. Those receiving methamphetamine detoxification were treated with supportive therapy.

Sera were tested for HIV by enzyme-linked immuosorbent assay (Vironostica HIV Uni-form II plus 0; Organon Teknika, Research Triangle Park, North Carolina, USA). Reactive specimens were tested with gel-particle agglutination (GPA) tests, (Serodia-HIV; Fujirebio Inc., Tokyo, Japan). Sera positive in both assays were considered HIV positive. GPA-non-reactive specimens were confirmed by Western blot (HIV Blot 2.2; Genelabs Diagnostics, Singapore). Syphilis antibodies were detected by a rapid plasma reagin (RPR) (SyphScreen; Shield Diagnostics, London, UK), and reactive specimens were confirmed by a Serodia-TP-PA (Funirebio Inc., Tokyo, Japan). Chlamydia and gonorrhea were detected using polymerase chain reaction (Amplicor PCR Diagnostics; Roche Diagnostics Systems, Inc., Branchburg, New Jersey, USA).

The data were analyzed using χ², Mantel-Haenszel χ² test for trends, and multiple logistic regression to estimate the unadjusted and adjusted odds ratios (OR) and 95% confidence intervals (CI) associated with MSM behaviors versus only female sex partners, and for HIV infection.

Results

A total of 1752 (84.7%) of the 2005 males in drug treatment reported having ever had sex, and 66 of 1752 (3.8%) reported ever having sex with another man and/or Katoey. In comparison with all other sexually active men, the MSM were significantly more likely to have HIV infection on admission for drug treatment (OR, 2.3; 95% CI, 1.4-4.0), than were HM. Forty-six of the 66 MSM (70%) reported past or current injection drug use.

Sex partners

MSM were significantly younger with a median age of 25 years compared to HM, with a median of 30 years (P = 0.002). Despite their comparative youth, MSM had significantly higher numbers of lifetime sexual partners, a median of 20, than HM, who had a median of 6 (P = 0.0001). MSM also reported more female sex partners in the past year (mean, 2) than did HM (P = 0.002); reported more female paid sex partners (P < 0.0001), and were more likely to have been paid for sex (P < 0.0001) (Table 1).

Table 1

Among the 66 men reporting at least one lifetime male sex partner, 59 (89.4%) reported having had a Katoey partner. Other partners were uncommon: four had a steady male partner; and five reported casual male partners. Three men reported both male and Katoey partners and seven (10.6%) reported only male-identified partners. The large majority, 56 men (84.8% of MSM) reported exclusively Katoey partners.

Demographic, behavioral and drug use risks

Table 1 compares MSM with HM. MSM were much more likely to be ethnic Thais, (P < 0.0001) were younger, and better educated.

MSM men were more likely to have traded sex for money (P < 0.0001) and to have traded sex for drugs (P < 0.0001) (Table 1). They were also more likely to have had Fang Muk, the Thai traditional penile implants (P < 0.0001) [Fang Muk are pearls, pieces of jade, or glass or metal beads inserted into the skin of the penis and/or foreskin. They are traditional in Thailand and are meant to enhance stimulation for a man's sex partners.].

MSM were more likely to have ever injected drugs than HM (P < 0.0001), to have sold drugs (P < 0.0001), been in prison (P < 0.0001), to have injected drugs in prison (P < 0.0001), and to have ever used heroin and opium. They were not more likely to have used methamphetamine.

Comparing MSM and HM among all men with a lifetime injection drug use (IDU) history, MSM-IDU were younger than other IDU (P < 0.0001), more likely to be Thai (P < 0.001), reported greater numbers of lifetime sexual partners (P < 0.001), had sex with female sex workers (P < 0.001), traded sex for money and for drugs, had ever been in jail/prison (P < 0.0001) and injected drugs in prison (P < 0.01).

Biologic correlates

MSM were significantly more likely to be HIV infected on admission for treatment than were HM, with 21 of 66 MSM being HIV infected (31.8%), compared with 282 of 1686 (16.2%) of HM (OR, 2.32; 95% CI, 1.36-3.96). MSM also had higher HCV prevalence with 65.2% of MSM being HCV positive compared with 41.9% of HM (OR, 2.59; 95% CI, 1.55-4.34). Sexually transmitted disease rates did not differ.

In a multivariate logistic regression analysis comparing MSM with all other sexually active male drug users, younger age, Thai ethnicity, greater number of lifetime sex partners, ever trading sex for money, and having a penile implant all remained independently associated with MSM behaviour (Table 2). Injection drug history, having been incarcerated, and being HIV infected were not independent predictors of MSM status.

Table 2

HIV knowledge and attitudes

MSM had high knowledge of HIV infection and prevention and were more likely to report having had an HIV test prior to admission than other men (P < 0.0001). They were more likely to agree with the statement that condoms reduced sexual pleasure (P < 0.0001), and that condoms were effective for HIV prevention (P < 0.01) and do not often break or leak during sex (P < 0.001). MSM were mistakenly more likely to agree that withdrawal before ejaculation can prevent HIV infection (P < 0.001).

Discussion and conclusions

Northern Thai MSM who attend for drug treatment have strikingly different sexual behaviors and risks from MSM populations reported in other cultural settings. The majority, 56 of 66 (84.8%) reported only having had Katoey, or male transgendered partners, among their male partners, and overall 59 (89.4%) had at least one lifetime Katoey partner. These MSM had a greater numbers of female sex partners, and greater numbers of female sex-worker partners, than drug using HM. Independent associations with MSM behaviors included greater numbers of lifetime sex partners (male, female and Katoey), having sold sex for money, and having a traditional penile insert. These risk patterns and behaviors describe a group of men with marked substance use risks, multiple sex partner types and high rates of sexual risks. In earlier ethnographic work among Royal Thai Army conscripts, we found that men who reported only Katoey male partners perceived of themselves as 'Puchai' men, and as having a male gender orientation and dominant sexual roles ^[11]. This cultural pattern has been remarkably little studied: a Medline search (on 12 February 2005) on the term 'Katoey' yielded no scientific publications-a 'Google' search on the same term (on 12 February 2005) yielded 25 600 results including bars, clubs, cabaret shows, dating services, and chat rooms dedicated to Thai Katoey. Although HIV and sexual health research may have overlooked Katoey, the sex and tourism industries have not.

Since Thai drug users are commonly incarcerated, a concern here was the potential for situational homosexual behavior in jails, prisons, or single-sex drug treatment settings to have over-estimated the associations with same-sex behavior and substance use. The cross-sectional nature of this study makes causal interpretations between a history of sex with men and a history of prison impossible. However, while MSM behaviors were associated with incarceration in univariate analysis, incarceration did not remain independently associated with a lifetime history of MSM behaviors, suggesting that these men were not simply heterosexuals with a history of homosexuality in prison. A further analysis looking at MSM drug users who reported male, but not Katoey partners, did not show a significant association with a history of incarceration and these behaviors (P = 0.19).

An additional limitation of this study is the absence of Katoey participants in the OUR cohort. While the majority of the MSM we studied reported Katoey partners, we do not have data on how many men (or women) self-identified as Katoey. Studies of HIV and other health concerns among Katoey are urgently needed to assess the prevention needs of these transgender men.

A large body of literature demonstrates the importance of targeted prevention strategies. A public health implication of this study is that prevention targeting Thai MSM must take into account divergent cultural forms of identity, gender and behavior. Encouraging findings here were that MSM drug users had high rates of HIV knowledge and awareness, and of their prior HIV testing history on treatment admission. The high rates of sexual and substance use risks in this group suggest that prevention remains a priority.

Acknowledgements

Sponsorship: This research was supported by a grant from the National Institute of Drug Abuse (R 01 DA11133), US National Institutes of Health, by the Fogarty International Center (DW43-00001) and by the Royal Thai Government.