Abstract
Female sex workers (FSWs) aged ≥18 years without known HIV infection living in Tijuana and Ciudad Juarez, Mexico who had recent unprotected sex with clients underwent interviews and testing for chlamydia and gonorrhoea using nucleic acid amplification. Correlates of each infection were identified with logistic regression. Among 798 FSWs, prevalence of chlamydia and gonorrhoea was 13.0% and 6.4%, respectively. Factors independently associated with chlamydia were younger age, working in Tijuana versus Ciudad Juarez and recent methamphetamine injection. Factors independently associated with gonorrhoea were working in Tijuana versus Ciudad Juarez, using illegal drugs before or during sex, and having a recent male partner who injects drugs. Chlamydia and gonorrhoea infection were more closely associated with FSWs' drug use behaviours and that of their sexual partners than with sexual behaviours. Prevention should focus on subgroups of FSWs and their partners who use methamphetamine and who inject drugs.
INTRODUCTION
Tijuana, Baja California and Ciudad Juarez, Chihuahua lie on Mexico's border with the USA and are characterized by large populations of migrants and female sex workers (FSWs). Both cities have ‘zones of tolerance’ where sex work is quasilegal. Clients include men from both sides of the USA–Mexico border and from other countries, ranging in age from 18–80 years old. 1,2 In 2006, it was reported that 4850 Tijuana FSWs were registered with the Municipal Health Service, while thousands of others are thought to work without a permit. 3 Approximately 4000 FSWs work in zones of tolerance of Ciudad Juarez, where sex work is not regulated by the Health Department. 3
Prevalence estimates for chlamydia and gonorrhoea among FSWs in Mexico have been reported in a few studies. 4,5 However, data are sparse among FSWs who reside near the Mexico–USA border. Among 354 registered FSWs in three northern non-border Mexican cities (Durango, Durango; Zacatecas, Zacatecas; and Torreón, Coahuila), the prevalence of cervical Chlamydia trachomatis infection was 12.4%. 6 In a 1993 study among 826 sex workers in Mexico City, 3.7% tested positive for gonorrhoea. 4
Chlamydia and gonorrhoea share some risk factors, such as female gender, younger age at sexual debut, low contraceptive use, greater number of sexual partners, engaging in commercial sex work and drug use. 7–12 Recent studies have also identified partner-level risk factors; for example, in a sample of 15–24 year olds, partners who had a sexually transmitted infection (STI) in the past year and partnerships with an age difference of five years or more were more predictive of STIs than were the individuals' own sexual behaviours. 13 STI risks may also differ by sexual partner type. Among 553 high-risk heterosexual women in Houston, TX, condom use was higher with casual partners than with steady partners; however, this advantage was reversed when alcohol, drugs or both were used. 14
Although the number of studies has been fewer, there has been some research on partner-level characteristics that may influence STI acquisition in countries or communities that are specifically low- or middle-income. For example, a study of 4000 married or co-habiting men living in Mexico City found that those having extra-relational sex in the last year were more likely to use condoms with their secondary partners (e.g. FSWs) than with their primary partners. 15
In Mexico, certain population subgroups show high prevalence of chlamydia and gonorrhoea varying by region. 16,17 Of particular interest for our study was that women in communities along the border between Arizona and the Mexican state of Sonora were at significantly increased risk for chlamydia infection compared with women attending clinics in non-border locations (9.0% versus 5.4%). Testing positive for chlamydia was associated with younger age, a history of new sexual partner(s) in the previous three months and proximity to the international border. 18
Major drug trafficking routes for heroin, cocaine and methamphetamine pass through both Tijuana and Ciudad Juarez. We previously reported that FSWs in these cities who injected drugs had higher overall STI prevalence and engaged in more unsafe sex with clients compared with FSWs who did not inject drugs. 19 In addition, FSWs with USA clients were significantly more likely to inject drugs, have unprotected sex for more money and to have recently tested positive for one of four STIs (gonorrhoea, chlamydia, HIV, active syphilis) compared with other FSWs. 20 However, in that study we did not examine individual- or partner-level risk factors for STI acquisition, nor did we examine risk factors for gonorrhoea and chlamydia separately. In the present analysis, we examine whether FSWs testing positive for gonorrhoea and chlamydia report higher rates of drug use before or during sex and whether partner-level characteristics are closely associated with these incident STIs. In a resource-limited setting such as Mexico, identifying correlates of STIs is important for targeting funding for STI screening and treatment.
MATERIALS AND METHODS
Study population
From March 2004 to January 2006, FSWs in Tijuana (n = 474) and Ciudad Juarez (n = 450) were recruited into a behavioural intervention study described previously. 21 Participants were women who were at least 18 years old who had traded sex for drugs, money or other material benefit and reported having had unprotected vaginal or anal sex with a client at least once during the previous four weeks.
Measures
Data were collected during a private interview. Measures included demographics, sexual behaviours, substance use, male client characteristics and test results for chlamydia, gonorrhoea, syphilis antibodies and HIV antibodies. Data were restricted to the baseline visit.
Demographic characteristics
Sociodemographics included current age, age at initiation into sex work, marital status, having children, city of residence, place of birth and type of sex work (street worker, dance hostess, barmaid, other).
Sexual behaviours
Condom use was assessed by the following: whether participants had condoms with them at the interview; total number of sex acts and of unprotected sex acts in the past six months, broken down according to partner type (spouse or steady; any client; non-regular clients; regular clients); average amount (US$) paid by clients for protected and unprotected sex; and frequency of condom use for vaginal sex with male clients (never or sometimes versus often or always). The ratio of the total number of sex acts to unprotected sex acts in the past six months were used to calculate the percentage of unprotected vaginal sex for each partner type.
Substance use
Each participant was asked whether she had used alcohol or an illegal drug before or during sex during the past month; had ever injected cocaine, heroin, methamphetamine, speedball or any illicit drug; the number of sex partners in the past month who were injection drug user (IDU); the number of male clients in the past six months who (to the FSW's knowledge) had ever injected drugs; and whether the participant had ever shared needles or injection equipment with anyone.
Male client characteristics
We assessed number, type (regular and non-regular) and perceived origin (USA or Mexico) of male clients, as well as the number of vaginal sex acts with clients of each type.
Chlamydia, gonorrhoea, syphilis and HIV
Cervical swabs were prepared and tested with nucleic acid amplification using the Aptima® Combo 2 assay collection device (GenProbe, San Diego, CA, USA) to detect Neisseria gonorrhoeae and C. trachomatis. From a blood sample, HIV antibody was detected on site using the Determine® rapid HIV antibody test (Abbott Pharmaceuticals, Boston, MA, USA); reactive samples were confirmed by enzyme immunoassay and Western blot. The rapid plasma reagin (RPR) test was used to detect syphilis antibody (Macro-Vue, Becton Dickenson, Cockeysville, MD, USA); reactive samples were confirmed by Treponema pallidum haemagglutination assay (Fujirebio, Wilmington, DE, USA). RPR titres >1:8 were considered consistent with active infection. 22
Statistical analysis
Bivariate associations by chlamydia and gonorrhoea infection were performed with non-parametric Fisher's exact test and Wilcoxon's two-sample test, as appropriate.
Logistic regression was performed to identify factors associated with chlamydia and gonorrhoea infections. In multivariate regressions, all variables attaining a significance of P < 0.10 in bivariate analysis were considered for inclusion; models were reduced manually using stepwise regression and the likelihood ratio test (P < 0.05). Factors with medium-to-high Spearman correlation (r > 0.6) were not included in the same model. A tolerance test was performed on the final model to assess multicollinearity.
RESULTS
Of 924 participants, 126 had samples that were spoilt due to extreme heat and border crossing delays; their chlamydia and gonorrhoea test results were thus excluded. Women who were excluded for this reason were significantly older, more likely to be from Ciudad Juarez and to be street workers, were less likely to be migrants, reported significantly less unprotected vaginal sex with any type of client and earned less for sex with and without a condom. Of the 798 remaining, 466 (58.4%) worked in Tijuana and 332 (41.6%) in Ciudad Juarez. The median age was 32 years (interquartile range [IQR]: 26, 39); 17.8% had ever injected drugs; and the median number of clients in the past six months was 240 (IQR: 72, 480). Overall, 104 (13.0%) tested positive for chlamydia, and 51 (6.4%) tested positive for gonorrhoea.
Factors associated with chlamydia infection
FSWs who tested positive for chlamydia were significantly younger and more likely to be living in Tijuana than in Ciudad Juarez. We did not find differences by chlamydia infection with respect to their age of initiation into sex work, marital or migration status, sex worker type, condom use practices or male client characteristics (Table 1).
Factors associated with chlamydia infection among female sex workers in Tijuana and Ciudad Juarez (n = 798)
OR = odds ratio; CI = confidence interval; SD = standard deviation; USD = US dollar; IDU = injection drug user; STI = sexually transmitted infection
Note: The following variables were entered into the analysis, but were found not significant: under condom use: participant brought condoms to the interview (yes/no); used condoms for vaginal sex with male clients in the past six months (never or sometimes versus often or always). Under substance use: used alcohol before or during sex (never or sometimes versus often or always); used illegal drug before or during sex (never or sometimes versus often or always). None of the measured male client characteristics (e.g. number of male clients in the past six months) was found significant
Univariate statistics include: mean (SD) and Wilcoxon test P value for continuous variables, and N (%) and Fisher exact test P value for categorical variables
*Per 10 unit increase
OR (CI) values that are significant are shown in
FSWs who tested positive for chlamydia had higher lifetime prevalence of injecting drugs (29% versus 16%), and were more likely to have ever shared needles or injection equipment (23% versus 12%), or injected heroin (26% versus 14%), or methamphetamine (10% versus 3%) in the past month. We did not find significant differences with respect to alcohol or illegal drug use before or during sex, injecting cocaine or speedball in the previous month, or number of IDU sex partners in the past month. Not surprisingly, FSWs with chlamydia infection also had significantly higher prevalence of HIV (15% versus 4%), active syphilis (titre >1:8) (18% versus 9%) and gonorrhoea (19% versus 4%).
Factors independently associated with chlamydia were being younger (adjusted odds ratio [AOR]: 0.63; 95% confidence interval [CI]: 0.48, 0.82 per 10 years), working in Tijuana versus Ciudad Juarez (AOR: 2.34; 95% CI: 1.43, 3.83) and having injected methamphetamine in the past month (AOR: 2.68; 95% CI: 1.18, 6.05) (Table 2).
Characteristics independently associated with chlamydia and gonorrhoea infection among female sex workers
AOR = adjusted odds ratio; CI = confidence interval; IDU = injection drug user
Factors associated with gonorrhoea infection
Factors associated with gonorrhoea infection among FSWs in Tijuana and Ciudad Juarez included substance use, certain client characteristics and having other STIs.
FSWs with gonorrhoea infection were over four times more likely to work in Tijuana than in Ciudad Juarez. We detected no associations between gonorrhoea infection and age, age of initiation into sex work, marital status, having children, migration, sex worker type or condom use practices (Table 3).
Factors associated with gonorrhoea infection among female sex workers in Tijuana and Ciudad Juarez (n = 798)
OR = odds ratio; CI = confidence interval; SD = standard deviation; USD = US dollar; IDU = injection drug user; STI = sexually transmitted infection
Note: See note to Table 1. The same variables were omitted from Table 3
Univariate statistics include: mean (SD) and Wilcoxon test P value for continuous variables, and n (%) and Fisher exact test P value for categorical variables
*Per 10 unit increase
OR (CI) values that are significant are shown in
FSWs with gonorrhoea infection were more likely to have often or always used illegal drugs before or during sex, to have ever injected drugs and to have ever shared needles or injection equipment. Those testing positive had significantly higher lifetime prevalence of drug injection (43% versus 16%) as well as injection in the past month of cocaine (15% versus 6%), heroin (37% versus 14%), methamphetamine (16% versus 3%) and speedball (14% versus 6%) (Table 3). We did not find associations with alcohol use before or during sex, or the number of IDU sex partners.
FSWs with gonorrhoea had significantly fewer non-regular clients in the past month, but had significantly more vaginal sex with these clients. They were also more likely to report having a male client who had ever injected drugs or a USA client. We found no association between gonorrhoea and number of male clients, vaginal sex with regular male clients or sharing needles with clients. FSWs with gonorrhoea had significantly higher prevalence of HIV (22% versus 4%), active syphilis (titre >1:8) (36% versus 8%) and chlamydia (39% versus 11%).
Factors independently associated with gonorrhoea infection were working in Tijuana versus Ciudad Juarez (AOR: 4.75; 95% CI: 1.80, 12.52), use of illegal drugs before or during sex (AOR: 5.96; 95% CI: 3.01, 11.80) and having a male IDU partner in the past six months (AOR: 2.32; 95% CI: 1.16, 4.63) (Table 2).
DISCUSSION
In this study of high-risk FSWs residing in two Mexico–USA border cities, chlamydia and gonorrhoea were more closely associated with drug use among FSWs and their sexual partners than with FSWs' sexual behaviours. Specifically, use of illegal drugs before or during sex and having male IDU clients were independently associated with gonorrhoea infection, and recent methamphetamine injection was independently associated with chlamydia infection. Odds of chlamydia and gonorrhoea infection were two to four times higher in Tijuana than in Ciudad Juarez. These findings have implications for targeting STI prevention and treatment to subgroups of FSWs who use illicit drugs in these resource-limited settings, especially in Tijuana.
We found that methamphetamine injection was an independent predictor of chlamydia infection. Use of methamphetamine has been associated with increased libido and numbers of sexual partners, as well as with high-risk sexual behaviour. 23–26
Although methamphetamine use is becoming more common among heterosexual women in countries such as the USA, the high prevalence of methamphetamine injection in our sample (21%) is unusual.
While gonorrhoea infection was not associated with the use of methamphetamine or other drug types, it was independently associated with using an illegal drug before or during sex. A critical review of 16 epidemiological studies associated drug use with increasing rates of STIs, including gonorrhoea. 27 Other studies have documented an association between substance use and lower rates of condom use or impaired ability to use condoms. 14,28 Some of the authors have initiated a new intervention study that aims to promote skills in negotiating condom use among FSWs in Tijuana and Ciudad Juarez who inject drugs, and we hope this will lead to a significant reduction in HIV/STI incidence.
Having an IDU sex partner in the past six months was the only partner-level variable to be associated with incident STIs in our study, and this relationship was observed only for gonorrhoea. The lack of independent association of chlamydia and gonorrhoea with other partner characteristics may be due to limited study power, and the fact that women were asked to report their partner characteristics. Future studies should consider obtaining such data directly from FSWs' clients and intimate partners, since FSWs' reports of their partners may not be a suitable proxy.
Our results support the existing literature linking younger age with chlamydia infection. In a systematic review of risk factors for chlamydia among women in the UK and Ireland, younger age was one of the most important determinants. 29 Our findings reinforce the need for increased screening for chlamydia among young FSWs, especially those who inject methamphetamine.
Interpretation of these findings should consider a number of limitations. First, we relied on the accuracy of self-report, which could result in under-reporting, especially for variables relating to partner characteristics. Further, given that data were gathered as part of an intervention study to reduce sexual risk, only women reporting recent unsafe sex were included, which may have biased associations with condom use towards the null. Specimen spoilage led us to exclude samples from 126 FSWs, some of whom appear to have been at higher risk. This may have caused some selection bias that influenced our results in unanticipated ways; however, this would tend to affect external validity and not the internal validity of our findings. Finally, since this analysis was cross-sectional, no causal inferences can be drawn; however, since nucleic acid amplification detected active infection, the variables we found to be associated with chlamydia and gonorrhoea may be true risk factors.
Given that both chlamydia and gonorrhoea are co-factors of HIV transmission, 30 there is a need to scale up interventions to increase testing, diagnosis and treatment for STIs, especially among drug-using FSWs and their partners in these cities. Since Tijuana and Ciudad Juarez are experiencing rising rates of HIV infection among FSWs, 31,32 identifying and intervening on risk factors for chlamydia and gonorrhoea have implications not only for STI control, but also for containing the burgeoning HIV epidemic.
Footnotes
Acknowledgements
This research was made possible with support from NIH Grants R01MH065849, R01DA023877, DA019829-02S1 and 1K01 DA025504-01A1. The authors gratefully acknowledge the study staff and participants of Proyecto Mujer Segura, Brian Kelly for editing assistance, and the following organizations for their cooperation: the Municipal and State Health Departments of Tijuana, Baja California and Ciudad Juárez, Chihuahua; Salud y Desarollo Comunitario de Ciudad Juárez A.C. (SADEC), Patronato Pro-COMUSIDA, and Federación Méxicana de Asociaciones Privadas (FEMAP); and the Universidad Autónoma de Baja California (UABC) and Universidad Autónoma de Ciudad Juárez (UACJ). In addition, we would like to thank the County Health Departments of San Diego, CA and El Paso, TX for their assistance with STI and HIV testing. O L also gratefully acknowledges her dissertation committee: V D O from the University of California at San Diego and Sue Lindsay and Ming Ji from San Diego State University.
