Background: Research has focused on male clients of female sex workers (FSWs) and their risk for HIV/sexually transmitted infections (STIs). However, it is unclear whether the commercial sex behaviors of these men are limited to paying for sex or whether they may also be paid for sex themselves.
Methods: We analyzed the interview data and HIV/STI test results from 170 drug-using male clients of FSWs in Tijuana, Mexico, to determine the extent to which these men report being paid for sex and the association with positive HIV/STI results.
Results: More than one quarter of men reported having been paid for sex in the past 4 months. In a multivariate logistic regression model, reporting having been paid for sex was significantly associated with testing positive for any HIV/STI (adjusted odds ratio [AdjOR], 3.53; 95% confidence interval [CI], 1.33–9.35), being bisexual (AdjOR, 15.59; 95% CI, 4.81–50.53), injection drug use in the past 4 months (AdjOR, 2.65; 95% CI, 1.16–6.03), and cocaine use in the past 4 months (AdjOR, 2.93; 95% CI, 1.22–7.01).
Conclusions: Findings suggest that drug-using male clients of FSWs may be characterized by unique risk profiles that require tailored HIV prevention interventions.
In a study of drug-using male clients of female sex workers, 26.5% reported also having been paid for sex. HIV/sexually transmitted infection&#x2013;positive clients were 3.5 times as likely to have been paid for sex as HIV/sexually transmitted infection&#x2013;negative clients.
From the *Division of Global Public Health, Department of Medicine, and †Department of Psychiatry, University of California San Diego, La Jolla, CA; and ‡Centro de Investigación en Infecciones de Transmisión Sexual, Programa de Investigación de la Clínica Especializada Condesa Programa de SIDA de la Ciudad de México Secretaría de Salud del Distrito Federal, México DF, México
Acknowledgments: The authors thank the project staff who assisted in the data collection effort (Arturo Tornez Zamudio, Deyna Arellano, Alfonso Chavez Rivera, and Ma. De Los Angeles Ramirez) and the participants who shared their stories for this account.
Supported by the US National Institutes of Health (K01DA031031, R01DA029008, T32DA023356). The funders had no further role in the design or conduct of the study and in the decision to submit the manuscript for publication.
Conflict of interest: None declared.
Contributors: K.D.W. was responsible for the design of the study, data analysis, and drafting the final manuscript. E.V.P. contributed to the conceptualization of the analysis and preparation of the manuscript. C.V.C. was responsible for overseeing the data collection and contributed to the preparation of the manuscript. C.M.-R. provided guidance on the presentation of results. T.L.P. contributed to the design of the study, conceptualization of the analysis, and presentation of the results.
Correspondence: Karla D. Wagner, PhD, Division of Global Public Health, Department of Medicine, University of California San Diego, 9500 Gilman Drive MC 0849, La Jolla, CA 92093-0849. E-mail: firstname.lastname@example.org.
Received for publication November 5, 2012, and accepted April 3, 2013.
The commercial sex trade (i.e., trading sex for money, drugs, or other items of value) has an important influence on epidemics of HIV and other sexually transmitted infections (STIs). The burden of HIV among female sex workers (FSWs) is disproportionately high, indicating a need for the rapid scale up of interventions to prevent new HIV and STI infections.1,2 Interventions among FSWs have shown some success in reducing incident HIV/STI infections and rates of unprotected sex.3 However, a focus solely on intervening with FSWs may neglect important barriers and risk factors introduced by FSWs’ commercial clients.4 Clients are in a position to connect (or “bridge”) members of higher- and lower-risk networks through sexual and drug use contact with FSWs, spouses, other noncommercial partners and drug use contacts.5 Whereas research has focused on male clients of FSWs in terms of their risk behaviors with FSWs (e.g., Goldenberg et al.6) and, to some extent, their noncommercial partners,5 an important research question is whether the commercial sex behaviors of these men are limited to paying for sex alone or whether they may also be paid for sex themselves.
Men who have sex with FSWs exhibit higher HIV/STI risk than do men who do not. In a study of clients in Thailand, men who had both FSW and non-FSW sex partners were twice as likely to be HIV positive and 3 times as likely to have had another STI in the past year.7 These bridgers reported only 30% consistent condom use with their FSW partners and less than 1% consistent condom use with non-FSW partners. Likewise, half of male clients in Tijuana, Mexico, who had wives or steady female partners were found to be “bridgers,” that is, to report unprotected sex with both FSWs and their wives or partners.5 Importantly, male clients’ sexual contacts are not limited to female partners. In Australia, 4.6% of male clients of FSWs recruited from a sexual health clinic also reported 1 or more male sex partners in the past year.8 In 2 British studies, 36% and 9% of clients reported sexual contact with other men.9,10 Having both male and female sex partners may facilitate more connections between groups that would otherwise not come into contact (e.g., men who have sex with men and heterosexual women), when these groups become linked through the sexual behavior of male clients.
In a parallel line of research, male sex workers (MSWs) have also been found to be at risk for HIV and other STIs because of high numbers of sexual partners and inconsistent condom use.11 In an Indonesian study, HIV prevalence was 3.6% among MSWs; 14% reported sex with paying female clients and 65% reported sex with paying male clients.12 These men also reported sex with nonpaying female partners (31%) and nonpaying male partners (32%); 54% reported sex with both male and female partners.12 A study of MSWs in 3 Australian cities found that self-reported HIV prevalence was 6.6%.13 Eighty-four percent of the Australian MSWs reported being in a permanent sexual relationship with a male partner and 15% with a female partner.13
Alcohol and drug use seems to be common among both clients of FSWs and MSWs. Drug use, particularly drug use during sex, has been associated with increased odds of reporting unprotected sex6 and “bridging” behavior among male clients.5 In Australia, MSWs reported alcohol or drug consumption during 51% of commercial sex encounters.14 In Madrid, Spain, 16% of MSWs reported injection drug use, and HIV prevalence among injection drug-using (IDU) MSWs was 60% compared with 17% among non-IDU MSWs.15
Despite the findings that both male clients of FSWs and MSWs are at elevated risk for HIV through both sex and drug use and report a variety of sexual partner types including both paid and paying partners, very little research examining the overlap of these behaviors in a single population exists. To that end, the primary aim of the current study was to examine the extent to which drug-using male clients of FSWs have also been paid for sex. We hypothesized that men who reported paying partners (i.e., partners who paid them for sex) would report higher sexual and drug risks than men who did not report paying partners.
Our sample was recruited in Tijuana, Mexico, where sex work is tolerated in permitted zona roja (i.e., “red light district”). Previous work has found the prevalence of HIV, syphilis, gonorrhea, and chlamydia among male clients in Tijuana to be 4%, 2%, 2.5%, and 7.5%, respectively, rates comparable with FSWs in the region.4 Tijuana is located on the Mexico-US border, only 17 miles south of its sister city of San Diego, California. Situated on one of the world’s busiest land border crossings, Tijuana is characterized by high degrees of cross-border mobility and is a destination for US residents seeking drugs and commercial sex as well as migrants from Mexico and Central America.16 Understanding the characteristics of individuals who have the potential to connect sexual and drug-using networks both within Mexico and across the border has important implications for stemming the growing and dynamic HIV epidemic in this region.17 In addition, findings may help inform HIV/STI prevention efforts in other border regions.
Participants and Recruitment
Data for this analysis were collected as part of an ongoing cross-sectional study of social factors associated with HIV risk among drug-using male clients of FSWs in Tijuana, Mexico. Eligibility criteria included the following: being older than 18 years; reporting use of heroin, methamphetamine, or cocaine in the past 4 months; having paid or traded something of value for sex with an FSW in Tijuana in the past 4 months; and ability to speak English or Spanish. Participants were recruited by indigenous Spanish-speaking outreach workers who contacted men in areas of the Zona Roja characterized by sex work and invited them to return to the study field site to conduct a brief eligibility screener. Upon determination of eligibility, participants provided written informed consent and completed a computer-assisted personal interview administered by Spanish-speaking or bilingual interviewers, depending on the respondent’s preference. Respondents also provided biological specimens for testing for HIV, chlamydia, syphilis, and gonorrhea. After the interview, men were provided with referrals for services, including treatment of HIV/STIs, if appropriate. The institutional review boards of the University of California San Diego (United States) and el Colégio de la Frontera Norte (Mexico) approved all study procedures.
Demographic questions included the following: age, race/ethnicity, location of residence, deportation history, and marital status. Sexual orientation was assessed with a single self-report item. Drug use items assessed drug type, frequency of use, mode of administration, and, for IDUs, frequency of receptive syringe sharing. Sexual behavior items included asking the respondent to give the number of sexual partners in the past 4 months in each of the following categories: regular female (e.g., a girlfriend or spouse), casual female (i.e., someone you see only occasionally), paid female (i.e., a woman you paid for sex), paying female (i.e., a woman who paid you for sex), regular male, casual male, paid male, and paying male.
Biological specimens were collected to test for HIV/STIs. The protocol included testing for HIV, syphilis, Neisseria gonorrheae, and Chlamydia trachomatis. The Advanced Quality Rapid Anti-HIV (1 and 2) test was used to detect the presence of HIV antibodies. Reactive and indeterminate specimens were retested with a second rapid test and confirmed through HIV-1 and HIV-2 serum antibody enzyme immunoassay (EIA) and indirect fluorescent antibody tests. The One Step Syphilis test (IND Diagnostic Inc, Delta, Canada) was used to conduct syphilis serology. All reactive samples were subjected to the rapid plasma reagin test and the Treponema pallidum particle agglutination assay. Urine samples were tested using the Gen-Probe Aptima Combo 2 Assay for C. trachomatis and N. gonorrhoeae tests.
Our analysis plan was designed to address 3 aims: (1) to examine the prevalence of various sex partner types (e.g., male regular, male paying, female regular, female paying, etc.) reported by a sample of male clients of FSWs, (2) to determine the association between reporting different sex partner types and HIV/STI infection, and (3) to investigate the correlates of reporting paying sex partners. Because the total number of partners in each of the categories (i.e., regular female, regular casual, etc.) was small and highly skewed, we collapsed each partner type into a dichotomous indicator of whether or not the respondent named at least 1 partner of that type. Receptive syringe sharing was also dichotomized into any versus no syringe sharing. First, we calculated descriptive statistics for all independent variables of interest, including measures of frequency, central tendency, and dispersion. Second, we conducted bivariate analysis using logistic regression to determine the association between reporting any sexual partner in each of the 8 categories and having a positive HIV/STI test result. We collapsed the data for HIV, syphilis, chlamydia, and gonorrhea into a dichotomous indicator of any positive HIV/STI test result, owing to small numbers in some cells that diminished power for subsequent analyses. Third, based on the results from that analysis, we conducted bivariate and multivariate analyses to determine the factors associated with reporting any paying partners (male or female). Bivariate comparisons were made using logistic regression. Factors significant at the P < 0.10 level were entered into a multivariate logistic regression model. The final model retained only those independent variables achieving statistical significance at the P < 0.05 level.
Between June 2011 and August 2012, 170 drug-using male clients provided sociobehavioral and biological data for this analysis. Overall, participants had a mean (SD) age of 39 (10.1) years. Seventy-two percent lived in Mexico (vs. the United States), 42% reported having ever been deported from the United States, and 87% were Hispanic. A minority (13.9%) reported bisexual sexual orientation; 86.1% identified as heterosexual and none identified as homosexual. Nearly one third reported being married or in a common-law arrangement. Eighteen percent were tested positive for any HIV/STI; 8.4% were positive for syphilis (lifetime or current), 4.1% were positive for HIV, and 7.5% were positive for chlamydia (data not shown). None was positive for gonorrhea.
In terms of the various partner types reported, in addition to reporting at least 1 paid female partner (i.e., FSW), almost half (47.7%) reported having at least 1 regular noncommercial female partner in the past 4 months, whereas 57% reported at least 1 casual noncommercial female partner (Table 1). Five percent reported having at least 1 regular male partner, 7.7% reported having at least 1 casual male partner, and 2.9% reported having at least 1 MSW partner.
In terms of paying partners, 19.4% reported having at least 1 paying female partner and 13.5% reported having at least 1 paying male partner in the past 4 months (Table 1). Altogether, 45 (26.5%) male clients in this sample reported having any male or female paying partners. Of those, 24% (n = 11) reported having both male and female paying partners, 49% (n = 22) reported having only female paying partners, and 27% (n = 12) reported having only male paying partners (data not shown). Being positive for HIV/STIs was associated with reporting any female paying partners (odds ratio [OR], 2.54; 95% confidence interval [CI], 1.05–6.14) and the collapsed indicator of any male/female partners (OR, 3.07; 95% CI, 1.35–6.99) and was marginally associated with reporting any paying male partners (OR, 2.36; 95% CI, 0.87–6.37; P = 0.09).
Table 2 shows the results of the bivariate analysis investigating demographic, sexual, and drug use factors associated with reporting any male/female paying sex partners in the past 4 months. Reporting any paying partners was more likely among those who reported being bisexual (vs. heterosexual; OR, 14.57; 95% CI, 4.96–42.85), those who reported injection drug use in the past 4 months (OR, 2.78; 95% CI, 1.09–4.36), and those who used cocaine in the past 4 months (OR, 2.92; 95% CI, 1.40–6.10). In the final multivariate logistic regression model retaining only significant covariates, clients who were positive for any HIV/STI were 3.5 times as likely to report having paying partners (95% CI, 1.33–9.35; Table 3). Being bisexual (adjusted OR [AdjOR], 15.59; 95% CI, 4.81–50.53), injection drug use in the past 4 months (AdjOR, 2.65; 95% CI, 1.16–6.03), and cocaine use in the past 4 months (AdjOR, 2.93; 95% CI, 1.22–7.01) also remained independently associated with reporting any paying sexual partners.
In this sample of drug-using male clients of FSWs in Tijuana, more than one quarter reported that they had been paid or given something of value for sex in the previous 4 months. Although some research has found that MSWs report both paying and paid partners,12 to our knowledge, this is the first study to examine these behaviors in a sample of drug-using male clients of FSWs. Forty-five men in our sample reported having male and/or female paying partners in the past 4 months, and having paying partners was significantly associated with an increased likelihood of being positive for HIV/STIs.
The HIV/STI prevalence in our sample was relatively high compared with a sample of male clients recruited from a sexual health clinic in Australia, which found HIV, syphilis, gonorrhea, and chlamydia prevalence of 0.2%, 1%, 0.8%, and 1.8%, respectively.8 However, it was lower than the 10.9% found by a study in 3 Indian states.18 The prevalence in our study is fairly comparable with the HIV/STI prevalence of FSWs in Tijuana.19 In contrast, Mexico’s general population HIV prevalence is low at 0.3%,20 whereas studies among Mexican MSWs have found HIV prevalence rates ranging from 3% in Acapulco to 26% in Monterry.21
It is important to consider the additional risk conferred by the high levels of drug use reported by the men in our study. Nearly half of the drug-using clients in our study reported injection drug use in the past 4 months, and IDUs were nearly 3 times as likely to report having paying sexual partners during that period. This association may be indicative of elevated drug dependence that requires a reliable source of income for purchasing drugs. Injection drug use has also been reported as a correlate of HIV infection in other studies of male clients.22 Most of our respondents reported using methamphetamine in the past 4 months, which has been associated with elevated levels of sexual risk behavior and HIV/STIs among clients,4 FSWs,19 heterosexual men,23 and men who have sex with men.24,25 Interestingly, however, our analysis found cocaine use in the past 4 months to be independently associated with having paying partners. This may suggest that drug use is localized among various drug-using subgroups and that clients who are paid for sex in Tijuana are characterized by different drug use patterns than the general population. In a study of young heroin users in Hanoi, Vietnam, Clatts and colleagues26 found that MSWs were significantly more likely than male non–sex workers to report lifetime use of marijuana, 3,4-methylenedioxy-methylamphetamine, amphetamines, cocaine, and morphine. Although methamphetamine tends to be localized in the Western United States and Mexico27 and is quite common among clients of FSWs in Tijuana,6 a focus on other stimulant drugs such as cocaine may be necessary to reduce HIV/STI risk among particular subgroups. Among IDUs, injecting cocaine has been reported as a significant risk factor for HIV infection, due perhaps, in part, to the increased frequency of cocaine injection relative to other drugs.28 Crack cocaine injection has also been associated with increased risk for sexual transmission of HIV among IDUs.29 If it is the case that clients who are also paid for sex exhibit different drug use profiles than other drug-using clients, interventions tailored to different drug-using groups (e.g., cocaine injectors) may be required.
Some limitations of the current findings should be acknowledged. Our study was designed to recruit drug-using male clients, so our findings may not generalize to non–drug-using men. However, as others have shown, drug use is quite common in this population8 and is an independent risk factor for HIV infection.22 Owing to the cross-sectional nature of our design, we have no information about the life history of our respondents or the trajectory of the onset of various risk behaviors. Understanding the various pathways through which individuals initiate drug use and sex work could help guide intervention efforts because the order in which drugs and sex work are initiated can have important implications.30 Because of the small sample size, we were unable to investigate some differences such as differences by type of STI or type of paying partner. Larger studies will be required to elucidate more fine-grained differences. Finally, future studies using network approaches in which all sexual partners are enumerated and the characteristics of and connections between those individuals are elicited will help to enhance our understanding of the possible HIV/STI transmission dynamics in these drug and sex networks.
Although considerable research has been focused on FSWs to understand risk factors for HIV/STI infection, less attention has been paid to FSW’s commercial partners, although clients are thought to outnumber FSWs 50:1.31 Our findings suggest that, at least among drug-using men, the behaviors of male clients and MSWs may overlap in a distinct group of individuals who both pay for and are paid for sex. If condom use and sterile injection practices are inconsistent, men’s network position as bridges between groups provides the opportunity for HIV/STI transmission between various population subgroups. Our findings suggest that these men may be distinguished by a unique set of behavioral factors including injection drug use and cocaine use. More research will be required to investigate the other defining characteristics of this group. In addition, research into the characteristics of the sexual partners who paid or traded for sex with the men in this study and how men’s condom use and drug use varies depending on partner type will be needed. In the meantime, prevention efforts should focus globally on increasing condom availability in sex work venues; condom use skills among FSWs, MSWs, and their clients; and social norms influencing the acceptability of condom use in these venues. Interventions may need to be tailored to particular drug-using communities because drug preference may be a marker for other behavioral characteristics such as commercial sex work.
1. Talbott JR. Size matters: The number of prostitutes and the global HIV/AIDS pandemic. PLoS One 2007; 2: e543.
2. Baral S, Beyrer C, Muessig K, et al. Burden of HIV among female sex workers in low-income and middle-income countries: A systematic review and meta-analysis. Lancet Infect Dis 2012; 12: 538–549. Epub 2012/03/20.
3. Patterson TL, Mausbach B, Lozada R, et al. Efficacy of a brief behavioral intervention to promote condom use among female sex workers in Tijuana and Ciudad Juarez, Mexico. Am J Public Health 2008; 98: 2051–2057. Epub 2008/09/19.
4. Patterson TL, Goldenberg S, Gallardo M, et al. Correlates of HIV, sexually transmitted infections, and associated high-risk behaviors among male clients of female sex workers in Tijuana, Mexico. AIDS 2009; 23: 1765–1771.
5. Patterson TL, Volkmann T, Gallardo M, et al. Identifying the HIV transmission bridge: Which men are having unsafe sex with female sex workers and with their own wives or steady partners? J Aids 2012; 60: 414–420.
6. Goldenberg SM, Cruz MG, Strathdee SA, et al. Correlates of unprotected sex with female sex workers among male clients in Tijuana, Mexico. Sex Transm Dis 2010; 37: 319–324. Epub Jan 14.
7. Morris M, Podhisita C, Wawer MJ, et al. Bridge populations in the spread of HIV/AIDS in Thailand. AIDS 1996; 10: 1265–1271.
8. Coughlan E, Mindel A, Estcourt CS. Male clients of female commercial sex workers: HIV, STDs and risk behaviour. Int J STD AIDS 2001; 12: 665–669.
9. Faugier J, Cranfield S. Reaching male clients of female prostitutes—the challenge for HIV prevention. AIDS Care 1995; 7: S21–S32.
10. Day S, Ward H, Perrotta L. Prostitution and risk of HIV—male partners of female prostitutes. BMJ 1993; 307: 359–361.
11. Shaw SY, Emmanuel F, Adrien A, et al. The descriptive epidemiology of male sex workers in Pakistan: A biological and behavioural examination. Sex Transm Infect 2011; 87: 73–80.
12. Pisani E, Girault P, Gultom M, et al. HIV, syphilis infection, and sexual practices among transgenders, male sex workers, and other men who have sex with men in Jakarta, Indonesia. Sex Transm Infect 2004; 80: 536–540.
13. Minichiello V, Marino R, Browne J, et al. Male sex workers in three Australian cities: Socio-demographic and sex work characteristics. J Homosex 2001; 42: 29–51.
14. Minichiello V, Marino R, Khan MA, et al. Alcohol and drug use in Australian male sex workers: Its relationship to the safety outcome of the sex encounter. AIDS Care 2003; 15: 549–561.
15. Belza MJ, Llacer A, Mora R, et al. Sociodemographic characteristics and HIV risk behaviour patterns of male sex workers in Madrid, Spain. AIDS Care 2001; 13: 677–682.
16. Goldenberg S, Strathdee SA, Gallardo M, et al. “Over here, it’s just drugs, women and all the madness”: The HIV risk environment of clients of female sex workers in Tijuana, Mexico. Soc Sci Med 2011; 72: 1185–1192. Epub March 3.
17. Strathdee SA, Magis-Rodriguez C. Mexico’s evolving HIV epidemic. JAMA 2008; 300: 571–573.
18. Subramanian T, Gupte MD, Paranjape RS, et al. HIV, sexually transmitted infections and sexual behaviour of male clients of female sex workers in Andhra Pradesh, Tamil Nadu and Maharashtra, India: Results of a cross-sectional survey. AIDS 2008; 22: S69–S79.
19. Patterson TL, Semple SJ, Staines H, et al. Prevalence and correlates of HIV infection among female sex workers in 2 Mexico-US border cities. J Infect Dis 2008; 197: 728–732.
20. UNAIDS. Global report: UNAIDS report on the global AIDS epidemic. HIV/AIDS JUNPo, 2010.
21. Magis-Rodriguez C, Bravo-Garcia E, Gayet C, et al. HIV and AIDS in Mexico until 2008: Findings, trends and thoughts. CENSIDA, 2008.
22. Reilly KH, Wang J, Zhu Z, et al. HIV and associated risk factors among male clients of female sex workers in a Chinese border region. Sex Transm Dis 2012; 39: 750–755.
23. Semple SJ, Amaro H, Strathdee SA, et al. Ethnic differences in substance use, sexual risk behaviors, and psychosocial factors in a sample of heterosexual methamphetamine users. Subst Use Misuse 2009; 44: 1101–1120.
24. Drumright LN, Patterson TL, Strathdee SA. Club drugs as causal risk factors for HIV acquisition among men who have sex with men: A review. Subst Use Misuse 2006; 41: 1551–1601.
25. Shoptaw S, Reback CJ. Methamphetamine use and infectious disease–related behaviors in men who have sex with men: Implications for interventions. Addiction 2007; 102: 130–135.
26. Clatts MC, Giang LM, Goldsamt LA, et al. Male sex work and HIV risk among young heroin users in Hanoi, Vietnam. Sex Health 2007; 4: 261–267.
27. Shukla RK, Crump JL, Chrisco ES. An evolving problem: Methamphetamine production and trafficking in the United States. Int J Drug Policy 2012. Epub 2012/09/05.
28. Chaisson RE, Bacchetti P, Osmond D, et al. Cocaine use and HIV infection in intravenous drug users in San Francisco. JAMA 1989; 261: 561–565.
29. Booth RE, Watters JK, Chitwood DD. HIV risk-related sex behaviors among injection drug users, crack smokers, and injection drug users who smoke crack. Am J Public Health 1993; 83: 1144–1148. Epub 1993/08/01.
30. Morris MD, Lemus H, Wagner KD, et al. Factors associated with pathways toward concurrent sex work and injection drug use among female sex workers who inject drugs in Northern Mexico. Addiction 2013; 108: 161–170. Epub 2012/07/11.
© Copyright 2013 American Sexually Transmitted Diseases Association
31. Thomas RM. Sex work. In: Curtis H, ed. Promoting Sexual Health. London: British Medical Association Foundation for AIDS, 1992.