Sexually Transmitted Diseases:
Correlates of Unprotected Sex With Female Sex Workers Among Male Clients in Tijuana, Mexico
Goldenberg, Shira M. MSC*†; Gallardo Cruz, Manuel MD‡; Strathdee, Steffanie A. PHD*; Nguyen, Lucie MS*; Semple, Shirley J. PHD§¶; Patterson, Thomas L. PHD§¶
From the *Division of Global Public Health, Department of Medicine, University of California, San Diego, La Jolla, CA; †Joint Doctoral Program in Public Health, San Diego State University and University of California San Diego, San Diego, CA; ‡Instituto de Servicios Estatales de Salud Pública, Baja California, Mexico; §Department of Psychiatry, University of California, San Diego, La Jolla, CA; and ¶MIRECC, VA Medical Center, San Diego, CA
Supported by the UCSD Center for AIDS Research with funds from NIH P30AI036214 and an administrative supplement to NIH R01DA23877–01A1S1.
The content is the responsibility solely of the authors and does not necessarily represent the official views of the National Institute of Allergy and Infectious Diseases, the National Institute on Drug Abuse, or the National Institutes of Health.
Correspondence: Thomas L. Patterson, PhD, University of California, San Diego, Dept. of Psychiatry 0680, 9500 Gilman Drive, La Jolla, CA 92093–0680. E-mail: firstname.lastname@example.org.
Received for publication June 18, 2009, and accepted October 8, 2009.
Background: Tijuana, situated adjacent to San Diego, CA on the US-Mexico border, is experiencing an emerging HIV epidemic, with prevalence among female sex workers (FSWs) having risen in recent years from <1% to 6%. Comparable data on FSWs' clients are lacking. We explored correlates of unprotected sex with FSWs among male clients in Tijuana.
Methods: In 2008, males from San Diego (N = 189) and Tijuana (N = 211) aged 18 or older who had paid or traded for sex with a FSW in Tijuana during the past 4 months were recruited in Tijuana's red light district. Participants underwent psychosocial interviews, and were tested for HIV, syphilis (Treponema pallidum), gonorrhea (Neisseria gonorrhoeae), and Chlamydia (Chlamydia trachomatis).
Results: Of 394 men, median age was 36 years, 42.1% were married, and 39.3% were unemployed. Ethnic composition was 13.2% white, 79.4% Hispanic, and 7.4% black or other. Half (50.3%) reported unprotected vaginal or anal sex with FSWs in Tijuana in the past 4 months. High proportions reported using drugs during sex (66%), and 36% reported frequenting the same FSW. Factors independently associated with unprotected sex with FSWs were using drugs during sex, visiting the same FSW, being married, and being unemployed.
Conclusions: FSWs' clients represent a sexually transmitted infections/HIV transmission “bridge” through unprotected sex with FSWs, wives, and other partners. Tailored interventions to promote consistent condom use are needed for clients, especially within the context of drug use and ongoing relations with particular FSWs.
Tijuana, a city of 1.4 million that borders San Diego, CA, is experiencing an emerging HIV epidemic. Of Mexico's 32 states, Baja California has second highest cumulative HIV incidence.1 In 2006, as many as 1 in 116 persons aged 15 to 49 years in Tijuana was estimated to be HIV-infected.2 Among female sex workers (FSWs) in border cities like Tijuana and Ciudad Juarez, HIV prevalence has risen in the last decade from <1% to 6%.3,4
Many Mexican cities contain a Zona Roja (red light district), where FSWs work under municipal permits that require routine sexually transmitted infection (STI)/HIV testing, but in Tijuana, approximately half of the city's estimated 9000 FSWs work without permits. Tijuana's Zona Roja draws male sex tourists from the United States, Mexico, and other countries. The percentage of Tijuana residents who report ever having used an illegal drug is 3 times the national average, perhaps because Tijuana is located within a major drug trafficking corridor.5–7 Drug use, particularly methamphetamine use, is rife among Tijuana's FSWs and is closely associated with HIV infection.4
Male clients of FSWs play an important role in HIV epidemiology, as they constitute a potential “bridge” for HIV/STIs from high- to low-prevalence populations through unprotected sex with a variety of partners.8–12 Of married men in Mexico, 28% report extramarital sex, including contact with FSWs, while 30% to 70% of male migrants report sex with FSWs.13,14 In Tijuana, 69% of FSWs reported having US clients; these women were also more likely to engage in unprotected sex with clients, to inject drugs, and to have active syphilis, suggesting a strong basis for cross-border transmission.15 Despite these facts, the risk behaviors of FSWs' clients in Mexico have yet to be carefully studied. We recently reported an HIV prevalence of 4% among male clients of FSWs in Tijuana as well as high levels of unprotected sex.16 Previous studies have linked unprotected sex with FSWs to clients' occupations,17–19 drug and alcohol use,15,16,20 relationship to FSWs,21 marital status,22–24 and age.19,24,25 However, the direction of many of these associations has been inconsistent. This analysis explores correlates of unprotected sex with FSWs among their male clients in Tijuana.
MATERIALS AND METHODS
San Diego and Tijuana form the world's largest cross-border metropolis and host its busiest international land border crossing.26 Tijuana's Zona Roja, where sex work is officially tolerated, sits a few blocks from the US border. A majority of the city's FSWs work out of clubs, bars, cantinas, hotels, and on street corners there.
In 2008, males from San Diego (N = 189) and Tijuana (N = 211) aged 18 or older who had paid or traded for sex with a FSW in Tijuana during the past 4 months were recruited in Tijuana's Zona Roja, as previously described.16 Clients were approached and asked if they would be willing to participate in a survey of sexual behavior and receive free HIV/STI testing. Of 226 males approached, 133 agreed to be screened for eligibility; 65 did not meet study criteria, 11 refused to participate, and 57 participated. Referrals by touts and other clients brought 405 men to the research office; of these, 343 were eligible and agreed to participate. All participants provided written informed consent and were compensated $30 US. The study protocol was approved by Institutional Review Boards in the United States and Mexico.
Interviews were conducted in private offices in Spanish or English. The interview included questions on demographics, past and current sexual and drug using behaviors, and other factors hypothesized to be associated with HIV/STI risk among clients, such as the nature of their relationships with FSWs and other partner types. For example, clients who answered the question “How often do you go back to the same prostitute?” with “Fairly often” or “Very often” were classified as “Visits the same FSW.” Similarly, men who responded “Yes” to both “Do you have a wife or steady female sex partner (e.g., girlfriend)?” and “Is your (wife/steady partner/girlfriend) a prostitute or ex-prostitute?” were classified as “Has current steady FSW sex partner.” We also inquired about other recent sex partners by asking, “In the past 4 months, did you have any casual female sex partners who were not sex workers?” and “In the past 4 months, have you had anal or oral sex with a man?”
The “Determine” rapid test was administered to a single drop of blood to detect the presence of HIV antibodies (Abbott Pharmaceuticals, Boston, MA). All reactive samples were tested using HIV-1 antibody by EIA and Western Blot. Treponema pallidum serology used the rapid plasma reagin test (Macro-Vue, Becton Dickenson, Cockeysville, MD) using a single drop of blood. Urine samples were tested for the presence of Chlamydia trachomatis and Neisseria gonorrhoeae using DNA Strand Displacement Amplification. Results of rapid HIV and syphilis tests were provided immediately; Chlamydia, gonorrhea, and confirmatory HIV results were available after 1 month. Free treatment for C. trachomatis and N. gonorrhoeae was provided on-site; those testing positive for HIV or syphilis were referred to municipal health clinics in Tijuana for free medical care.
Clients who reported at least one episode of unprotected vaginal or anal sex with a FSW in Tijuana within the previous 4 months were compared to clients who did not. Wilcoxon rank sum tests were used for continuous variables and Fisher exact tests for dichotomous variables. Univariate and multivariate logistic regression compared the 2 groups. Multivariate models were developed using a manual procedure where all variables of interest with a significance level of less than 10% in a univariate analysis were considered in order of most to least significant. Nested models were compared using the likelihood ratio statistic, retaining variables that were significant at the 5% level. All 2-way interactions were explored for the variables retained in the final model.
Sociodemographic and Social-Structural Characteristics
Of the 400 clients enrolled, 6 had incomplete data for variables of interest and were excluded from the analysis. Of the remaining 394, 198 (50.3%) reported unprotected vaginal or anal sex with one or more FSWs in Tijuana in the past 4 months (Table 1). By design, nearly half of participants (41.1%) were born in the United States and 57.1% were born in Mexico. Most (79.4%) identified as Latino or Hispanic, 13.2% as white, and 7.4% were black or other. The median age was 36 (interquartile range, 28–44); median education level was 11 years. Almost 40% of participants were unemployed, with a disproportionate number of unemployed men in the unprotected versus the protected sex group (43.9% vs. 34.7%).
About 42% of participants were married or in a common-law relationship, with married clients being more likely to report unprotected sex with a FSW in the past 4 months (47.5% vs. 36.7%; P = 0.033). A larger proportion of clients in the group that reported unprotected sex versus those who reported consistently having protected sex with FSWs were living with a partner or spouse (29.8% vs. 21.4%; P = 0.065). Over half reported a history of incarceration, which was significantly more likely in the unprotected versus protected sex group (60.1% vs. 45.9%; P = 0.006).
Overall, over one-fourth (27.6%) reported a current sex partner other than a FSW or ex-FSW. Recent sex with a male partner was reported by 14.2%, which was significantly more likely among clients who reported unprotected sex with FSWs (21.2% vs. 7.1%; P < 0.001). Compared to clients who reported consistently having protected sex with FSWs, clients in the unprotected sex group were significantly younger the first time they had sex with a FSW (median, 18 vs. 20 years; P < 0.001) and had a higher number of FSW partners in the past 4 months (median, 4 vs. 3.5; P = 0.004). As well, a larger proportion of clients in the unprotected sex group reported having a current steady FSW sex partner (36.3% vs. 12.3%; P = 0.001) and visiting the same FSW (44.9% vs. 26.7%; P < 0.001).
Drug and Alcohol Use
The majority (88.1%) reported a history of illicit drug use, with a higher proportion of illicit drug users among men who reported unprotected compared with protected sex with FSWs (91.9% vs. 84.2%; P = 0.020). One quarter of participants reported a history of injection drug use, with a significantly higher proportion in the unprotected sex group (32.8% vs. 17.3%; P < 0.001). Heroin, cocaine, and methamphetamine was reported among 36.5%, 49.5% and 63.7% of the sample, respectively, with higher proportions of men who used these drugs in the unprotected versus the protected sex group. Among men who reported ever injecting drugs, three-quarters (n = 74) reported receptive needle sharing in the previous 4 months. High overall levels of use during sex of alcohol and drugs were reported, which were significantly elevated in the unprotected sex group; for example, 66.2% (n = 260) of clients reported that they were high during recent sex with a FSW, with 78.7% (n = 155) of those in the unprotected sex group reporting this behavior versus 53.6% (n = 105) in the protected sex group (P < 0.001).
HIV and Sexually Transmitted Infections
Overall, 54 clients (13.9%) tested positive for at least one STI or HIV, with no significant differences between the groups reporting unprotected versus protected sex with FSWs. Compared with clients who did not report unprotected sex, clients who did were more likely to report a recent STI or symptoms (21.7% vs. 12.7%; P = 0.031) and were more likely to report having had a previous STI.
Factors Associated With Recent Unprotected Sex With FSWs
As shown in Table 2, compared to men who reported consistently having protected sex with FSWs in the past 4 months, clients who reported unprotected sex were more likely to be married or common-law, be unemployed, and to have fewer years of education. They were also more likely to report a recent male sex partner as well as frequenting the same FSW.
Compared to men in the protected sex group, men who reported unprotected sex were also significantly more likely to report a history of injection drug use, with methamphetamine use conferring the strongest association (odds ratio [OR], 2.4). Men in the unprotected sex group were significantly more likely to report being under the influence of alcohol or drugs during sex; for example, they were 3.2 times more likely to report being high and 1.8 times more likely to report being drunk during sex with a FSW within the previous 4 months.
Factors Independently Associated With Recent Unprotected Sex With FSWs
A total of 4 factors were independently associated with recent unprotected sex with a FSW: recently being under the influence of drugs during sex with a FSW (Adjusted OR [AOR], 3.2; 95% confidence interval [CI], 2.00–4.96); visiting the same FSW (AOR, 2.3; 95% CI, 1.45–3.53); being married (AOR, 1.5; 95% CI, 1.00–2.35); and being unemployed (AOR, 1.6; 95% CI, 1.00–2.39) (Table 3).
Our data characterize clients of FSWs as a population at very high risk of acquiring and transmitting STIs and HIV through unprotected sex with FSWs and other partners. Approximately half of all participants reported at least one recent episode of unprotected sex with a FSW in Tijuana, and visiting the same FSW, being married, being unemployed, and being under the influence of drugs during sex with an FSW were all independently associated with unprotected sex with a FSW. These findings suggest that FSWs' clients in Tijuana's Zona Roja represent an STI and HIV transmission “bridge” from higher-risk groups (e.g., FSWs, MSM, IDU) to lower-risk groups (e.g., wives, girlfriends, casual female partners), playing an important role in HIV transmission dynamics in this region. Mexico's HIV epidemic has recently shifted from low-level to concentrated3; however, widespread, immediate, and effective STI and HIV prevention interventions targeted toward high-risk subpopulations such as FSWs and their clients are needed to prevent a generalized epidemic. A modeling projection by Boily et al.27 found that in a concentrated epidemic, a 20% increase in condom use between FSWs and clients could reduce peak HIV prevalence by half and new infections by 21% over 1 year and 42% over 10 years.
Visiting the same FSW was independently associated with higher odds of having recent unprotected sex with a FSW. Research from other contexts suggests that condom use between FSWs and clients increases with social distance between partners, as FSWs are more likely to use condoms with casual or one-time clients. For example, a study of 403 FSWs' diaries in Kenya reported 69% condom use with “regular” clients and 90% with casual partners.28 HIV prevalence has also been shown to mirror these patterns, suggesting that sexual HIV transmission may be more strongly driven by sex with ongoing clients/regular partners rather than casual clients. In Canada, researchers found HIV infection among FSWs to be independently associated with unprotected sex with an intimate partner,29 while in Benin, a study documented HIV prevalence among casual clients, brothel personnel, and FSWs' boyfriends of 8.4%, 12.2%, and 16.1%, respectively.11 In Tijuana, ongoing interactions between clients and FSWs whom they regularly visit appear to blur the boundaries between commercial and interpersonal sexual relationships.30 This reinforces a comment made recently by one team that “the counterposition of high risk (sex work) and general population (noncommercial) can be counterproductive, reinforcing an idea that the exchange of cash is more likely to transmit infection than the exchange of love. For many people struggling to survive, the borderline between sex for convenience and for commerce is not clear.”31 As in other socially and economically marginalized communities, structural conditions in Tijuana also play a role; most FSWs live in poverty and are the sole supporters of immediate and extended family,5 making them prone to accept increased pay for unprotected sex.15
Being unemployed was independently associated with recent unprotected sex with a FSW. Unemployment can be seen as a marker of social and economic marginalization (not merely “lack of work”) that has been widely shown to contribute to HIV risk. “Unemployed” clients are more likely to live in “riskier” neighborhoods where they come into regular contact with FSWs and drugs. This finding adds to research that suggests strong linkages between socioeconomic disadvantage and HIV risk, both generally31 and among FSWs' clients.24
Being married was also independently associated with unprotected sex with a FSW—a highly concerning finding due to the risks conferred to potentially unknowing spouses (as well as other partners). Mixed findings exist regarding clients' marital status and condom use with FSWs in other contexts. Our study is consistent with findings from Tanzania, where unmarried clients were more likely to use a condom22; conversely, in the United States, married clients were more likely to use condoms with extramarital partners.25 Among our participants, it is possible that married men were more likely to have unprotected sex since they generally do not use condoms with their wives and may lack experience using and carrying them. These findings suggest that interventions must take clients' marital status and condom use with various partner types into account. In some contexts, condom promotion among clients of FSWs has been less successful than hoped for due to the challenges posed by high numbers of multiple noncommercial partners (e.g., interventions did not adequately address the need to use condoms with noncommercial partners).22,32,33 Promising mechanisms to address such challenges include condom promotion messages that are tailored to social and cultural contexts associated with different partner types and sexual behaviors. In Mexico, social norms heavily value male responsibility for ensuring the well-being of his family.13 Messages to encourage condom use among married clients could therefore incorporate such cultural underpinnings, by stressing the importance of protecting the health of one's family by consistently using condoms.
Drug use during sex was also independently associated with unprotected sex with FSWs by men in our sample, which is consistent with research from other countries.17,34–36 For example, among FSWs in Canada, drug sharing with clients was independently associated with such harms as inconsistent condom use by clients and the sharing of drug use paraphernalia.37 In cities along the US Mexico border, including Tijuana, we previously found that FSWs4 and clients16 who used methamphetamine were significantly more likely to be HIV-infected than their counterparts who did not use methamphetamine. In the current study, drug use during sex was more closely associated with unprotected sex than was history of methamphetamine use. Examining event-level data in greater detail and in conjunction with qualitative data may provide more meaningful explanations for clients' risk behaviors. Such data could support the development of interventions that appropriately address the concomitant risks of unprotected sex and heavy drug and alcohol use during sex among clients and FSWs.
While causal inferences cannot be drawn due to our study's cross-sectional design, our findings warrant further investigation and the development of interventions tailored to the needs of FSWs' clients. The use of self-reported data raises the possibility of reporting bias; indeed, follow-up qualitative interviews with a subsample of clients suggested that “undesirable” behaviors may have been underreported. Furthermore, our sample is not likely to be representative of more affluent “sex tourists.” Our outreach workers and local FSWs noted fewer visitors to the Zona Roja than expected during our recruitment period, which they attributed to escalating levels of violence in Tijuana. Thus, our sample may disproportionately reflect the experiences of “riskier” clients (who continued visiting the area), especially those who use drugs.
Clients of FSWs are a population known to be hard to reach and heterogeneous, and despite our best efforts to recruit a generalizable sample, ours may not be representative of clients outside of Tijuana's Zona Roja. However, since this neighborhood is where the majority of the city's FSWs congregate, these data signal the urgent need for cross-border client interventions. Future interventions should promote condom use for both US and Mexican clients with different partner types (e.g., spouses; FSW girlfriends) and within the context of drug and alcohol use.
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