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Sexually Transmitted Infections and Risk Behaviors Among African American Women Who Have Sex With Women: Does Sex With Men Make a Difference?

Muzny, Christina A. MD*†; Sunesara, Imran R. MBBS, MPH; Martin, David H. MD; Mena, Leandro A. MD, MPH

doi: 10.1097/OLQ.0b013e31822e6179
Original Study
Free

Objective: We sought to determine the prevalence of infection with Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis, Mycoplasma genitalium, syphilis, and HIV among African American women who have sex with women (AAWSW), and compare sociodemographics, sexual risk behavior characteristics, and STI diagnoses among women reporting sex exclusively with women (exclusive AAWSW) to women reporting sex with both women and men (AAWSWM) during the past 12 months.

Methods: Eligible women presenting to the Mississippi State Department of Health STD Clinic between February 2009 and October 2010 were invited to participate. A survey on sociodemographics, sexual history, and sexual risk behavior characteristics was completed. Women were tested for the presence of C. trachomatis, N. gonorrhoeae, T. vaginalis, M. genitalium, syphilis, and HIV.

Results: A total of 196 African American women were enrolled; 56.6% of all women reported engaging in sexual activity exclusively with women (AAWSW) during the past 12 months and 40.8% reported engaging in sexual activity with both men and women (AAWSWM). As compared with exclusive AAWSW, AAWSWM were significantly more likely to report prior infection with C. trachomatis (35.0% vs. 13.5%, P < 0.001), prior infection with N. gonorrhoeae (28.75% vs. 2.7%, P < 0.001), and transactional sex (18.8% vs. 2.7%, P = 0.001). Additionally, 13.8% of AAWSWM reported having sex with a homosexual or bisexual man during the past 12 months. Trichomoniasis was diagnosed in 18.3% of all women, C. trachomatis in 11.0%, M. genitalium in 7.6%, and N. gonorrhoeae in 3.7%. There were no cases of syphilis or HIV. AAWSWM were significantly more likely to be diagnosed with trichomoniasis (25.0% vs. 13.5%, P = 0.04), C. trachomatis (22.5% vs. 2.7%, P < 0.001), N. gonorrhoeae (7.5% vs. 0.9%, P = 0.01), or any STI (47.5% vs. 18.3%, P < 0.001) than exclusive AAWSW.

Conclusions: AAWSW in this study were at high risk for STI. AAWSWM, as a subgroup, may demonstrate heightened sexual risk-taking behaviors and higher STI rates compared with exclusive AAWSW. Sexual health services provided to AAWSW should take into account partner gender heterogeneity when counseling and screening for STI.

African American women reporting sex with women and men during the past 12 months demonstrated heightened sexual risk-taking behaviors and higher sexually transmitted infection rates compared with women reporting sex exclusively with other women.

From the *Division of Infectious Diseases, University of Alabama at Birmingham, Birmingham, AL; †Division of Infectious Diseases, University of Mississippi Medical Center, Jackson, MS; and ‡Division of Infectious Diseases, Louisiana State University Health Sciences Center, New Orleans, LA

The authors would like to thank Heather King, Tina Barnes, Tim Brown, Haitham Bhagdady, and the Crossroads Clinic nursing staff for their assistance in recruiting and enrolling patients for this study in addition to Craig Thompson in the Office of STD/HIV at the MSDH for his support of it. The authors would also like to thank Dr. Edward Hook, III, and Dr. Edwin Swiatlo for helpful discussions on manuscript preparation.

This study is registered at ClinicalTrials.gov, NCT 01043081.

Correspondence: Christina A. Muzny, MD, Department of Medicine, Division of Infectious Diseases, University of Alabama at Birmingham, ZRB 242-1530 3rd Ave, South Birmingham, AL 35294. E-mail: cmuzny@uab.edu.

Received for publication March 27, 2011, and accepted July 18, 2011.

Recent data from the 2006–2008 National Survey of Family Growth indicate that approximately 12.5% of American women aged 15 to 44 years engage in sexual activities with another woman at some point during their lifetime.1 Although a large body of research has focused on the sexual health of men who have sex with men because of the HIV/AIDS epidemic, far less has focused on the sexual and reproductive health needs of women who have sex with women (WSW).2 Among sexual minority groups, WSW are generally less vocal and less visible than men who have sex with men.

Historically, WSW are considered to be at low risk for STIs, including HIV.3–7 However, for the past 20 years, data from case reports,8–13 small prevalence studies,14–20 and surveys of self-reported history of STI among WSW21 have suggested that this generalization may not be correct. Assessment of STIs among WSW is complicated by the fact that some WSW also have a history of sex with men and continue to do so, putting themselves at risk for heterosexual acquisition of STIs and the potential for subsequent transmission to female sexual partner(s).22,23

To date, the majority of data regarding HIV/STI prevalence rates and sexual risk behaviors among WSW has been collected in whites. Little research is available that examines sexual risk behaviors and HIV/STI rates among African American WSW (AAWSW). It has been suggested that this group of women faces a “triple jeopardy,” in which individual stressors associated with race, gender, and sexual orientation compound and result in detrimental effects on their health.24 Likely as a result of facing such stressors, AAWSW report greater psychiatric morbidity than their heterosexual counterparts.25 Data from the 1960–1970s have shown that AAWSW may exhibit distinctive behavioral characteristics (e.g., more extensive heterosexual experiences) than their white counterparts that may put them at higher risk for HIV/STI acquisition.26,27 However, the extent of heterosexual experiences and burden of disease due to HIV/STI among AAWSW is largely unknown, especially among AAWSW living in the southern United States, where HIV/STI rates are especially high, and racial minority groups continue to face pronounced health disparities.28

To begin to address these knowledge deficits, the objectives of this study were to determine the prevalence of Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis, Mycoplasma genitalium, syphilis, and HIV among AAWSW living in an urban area in Mississippi and to compare the sociodemographics, sexual risk behavior characteristics, and STI diagnoses among those who reported having sex exclusively with women to those who reported engaging in sex with both women and men in the past 12 months.

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MATERIALS AND METHODS

Subjects

Between February 2009 and October 2010, we conducted a cross-sectional study that enrolled nonpregnant African American (AA) women aged ≥18 years who reported having sex with another woman within the past 12 months. Participants were recruited at the Mississippi State Department of Health (MSDH) STD clinic in Jackson, MS, as either a walk-in to the clinic or as a referral from a Women's Reproductive Health Program for sexual minority women sponsored by the clinic. Clients attended the Women's Reproductive Health Program as a result of notices distributed in lesbian and bisexual venues across town and through word of mouth. Women participating in this study were invited to refer their female sexual partners for possible enrollment.

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Definitions of WSW and Women Who Have Sex With Women and Men (WSWM)

For the purposes of this study, the term “WSW” applies only to sexual behavior, as all participants enrolled reported a history of sex with another woman within the preceding 12 months. Correspondingly, the term “WSWM,” when applicable, only applies to sexual behavior. The terms, as used here, are distinct from those referring to sexual orientation (synonymous with self-identification, usually discussed in terms of homosexuality [lesbian or gay], bisexuality, and heterosexuality), which may not necessarily be congruent with sexual behavior.29

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Procedures

After obtaining informed consent, participants were administered a written questionnaire containing questions on demographic and socioeconomic characteristics in addition to medical and sexual histories, including sexual risk behavior histories (past STI history, lifetime history of sex with men and sex with men in the past 12 months, lifetime number of female and male sexual partner(s) and number of female and male sexual partner(s) during the past 12 months, history of sexual contact with homosexual or bisexual men, history of sex in exchange for money or drugs, history of sexual contact with intravenous (IV) drug users, use of protective barriers during sexual activities [condoms with male sexual partners, condoms on sex toys, dental dams, etc.], alcohol/drug use at the most recent sexual encounter, and history of sex during menstruation). For the purpose of this study, “sex” was defined to include vaginal, oral, or anal sex.

A standardized physical examination was then performed by a study clinician that included visual inspection, palpation, and collection of vaginal fluid for pH measurement, saline microscopic examination, T. vaginalis InPouch culture (BioMed Diagnostics, White City, OR), N. gonorrhoeae and C. trachomatis detection using the Aptima Combo 2 assay (transcription-mediated amplification, GenProbe, San Diego, CA), and M. genitalium detection using a modified Aptima assay (research-only transcription-mediated amplification, Gen-Probe, San Diego, CA). Serum samples were collected for HIV and syphilis testing. HIV specimens were tested with a point-of-care test (Uni-Gold Recombigen HIV, Trinity Biotech, Co, Wicklow, Ireland) or the HIV-1 enzyme immunoassay (Bio-Rad Laboratories, Hercules, CA). HIV-1 Western Blot was available for confirmatory testing, if necessary (Bio-Rad Laboratories). Syphilis testing was performed using an in-house rapid plasma reagin test. Positive rapid plasma reagin tests were confirmed by a T. pallidum particle agglutination assay. Women were treated for STIs according to the 2006 Centers for Disease Control STD Treatment Guidelines30 and given a follow-up appointment in 2 weeks for all final test results and further administration of treatment, if necessary.

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Statistical Analysis

Statistical analysis was performed using SAS software v9.2 (SAS Institute, Cary, NC). Initial descriptive analyses for sociodemographic characteristics, sexual risk behaviors, and STI diagnoses were conducted for the entire cohort and later for the association among women who reported sex with men in the past 12 months. Associations between categorical variables were analyzed using chi-square or Fisher exact test, where appropriate. Continuous variables were compared between groups using the Wilcoxon 2-sample test. The 95% confidence interval for odds ratios was calculated. Stepwise logistic regression using backward elimination was used to build a multivariable model to describe independent predictors of the association of sex with men in the past 12 months. Variables that had a value of P ≤ 0.05 on univariate analysis were included (except for marital status, due to issues of convergence). Tests of significance were 2-tailed (P < 0.05). The study's procedures were reviewed and approved annually by the University of Mississippi Medical Center Institutional Research Board and the MSDH Institutional Research Board.

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RESULTS

Study Population

A total of 198 AAWSW were invited to participate in this study. Within this group of women, 2 refused to participate and 196 AAWSW were subsequently enrolled (Table 1). The study population was relatively young; mean age of participants was 24.5 (SD ± 5.0) and less than 15% were over 30 years of age. Only 25.0% (49/196) of all women reported having health insurance and only 21.4% (42/196) reported having a primary healthcare provider. Within the total group of women, 92.3% (181/196) reported on their sexual orientation, with 65.7% (119/181) self-identifying as homosexual and 32.6% (59/181) as bisexual. Lifetime history of sex with men was reported by 73.5% of women (144/196). Engaging in sex only with women (exclusive AAWSW) during the past 12 months was reported by 56.6% (111/196) of all women, whereas engaging in sexual activity with both women and men (AAWSWM) during the past 12 months was reported by 40.8% (80/196). We subsequently compared select demographic and socioeconomic characteristics between exclusive AAWSW and AAWSWM (Table 2). No significant differences between the 2 groups were found for age, education, household income, health insurance status, or having a primary healthcare provider. Exclusive AAWSW were significantly more likely to be involved in a long-term relationship than AAWSWM (P = 0.002).

TABLE 1

TABLE 1

TABLE 2

TABLE 2

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Risk Behavior Characteristics

Table 3 compares report of history of chlamydial infection, gonorrhea, trichomoniasis, syphilis, and HIV between exclusive AAWSW and AAWSWM. AAWSWM were significantly more likely to report a history of infection with C. trachomatis (35.0% vs. 13.5%, P < 0.001) and N. gonorrhoeae (28.75% vs. 2.7%, P < 0.001) than exclusive AAWSW. Although differences fell short of statistical significance, a higher proportion of AAWSWM reported prior infection with trichomoniasis (28.8%) than exclusive AAWSW (15.3%) (P = 0.05). There were no statistically significant differences between the 2 groups among the small proportion of women reporting prior infection with syphilis or HIV.

TABLE 3

TABLE 3

Table 4 compares select risk behaviors between the 2 groups of women. AAWSWM were significantly more likely than exclusive AAWSW to report a lifetime history of transactional sex (18.8% vs. 2.7%, P = 0.001). Although differences fell short of statistical significance, AAWSWM were more likely to report substance use (56.3% vs. 39.6%; P = 0.05) and alcohol use (71.3% vs. 56.8%; P = 0.06) within the past 30 days and less likely to report a history of consistent condom use on sex toys with female sexual partners (23.8% vs. 41.4%; P = 0.08) than exclusive AAWSW. There were no significant differences between the 2 groups regarding mean age at sexual debut with female or male partners, number of lifetime female sexual partners and number of female sexual partners within the past 12 months, tobacco use in the past 30 days, lifetime history of sex with an IV drug user, consistent barrier use at sexual exposure sites during the past 3 months (notably low at approximately 20% in both groups of women), or engaging in sexual activities with female partners during menstruation. Approximately 13.8% (11/80) of women in the AAWSWM group reported history of sex with a homosexual or bisexual man within the past 12 months (data not shown).

TABLE 4

TABLE 4

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STI Prevalence

At the time of evaluation, trichomoniasis was the most frequently diagnosed STI with 18.3% (35/191) of all women infected, followed by C. trachomatis at 11.0% (21/191), M. genitalium at 7.6% (14/191), and N. gonorrhoeae at 3.7% (7/191) (Table 5). No cases of pelvic inflammatory disease, syphilis, or HIV were diagnosed during this study. AAWSWM were significantly more likely to be diagnosed with trichomoniasis (25.0% vs. 13.5%, P = 0.04), C. trachomatis (22.5% vs. 2.7%, P < 0.001), N. gonorrhoeae (7.5% vs. 0.9%, P = 0.01), or any STI infection (47.5% vs. 18.3%, P < 0.001) than exclusive AAWSW.

TABLE 5

TABLE 5

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Multivariable Analysis

Significant findings from the multivariable analysis are shown in Table 6. We found that report of substance use within the past 30 days, history of gonorrhea infection, and new diagnosis of trichomoniasis and chlamydial infection were each independently associated with sex with a male partner(s) during the past 12 months.

TABLE 6

TABLE 6

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DISCUSSION

To our knowledge, this is the first study of STI prevalence rates and associated risk behaviors in a sample of AAWSW in the southern United States. Lifetime history of sex with men was common, consistent with previous studies of WSW reporting lifetime history of sex with men in 80% to 93% of participants,4,6,16,18–20,31–34 whereas the percentage of AAWSWM who had a male sex partner(s) within the past 12 months (40.8%) was somewhat higher than that seen in previous studies (6.7%–29.6%).6,18–20,34 Consistent barrier use at sexual exposure sites during the past 3 months was relatively low in both groups of women. Trichomoniasis was the most frequently diagnosed STI, followed by C. trachomatis, M. genitalium, and N. gonorrhoeae. No new cases of HIV or syphilis were diagnosed. In this study, infection rates with trichomoniasis and C. trachomatis were significantly higher than those seen in previously published studies of WSW and WSWM, which have ranged between 0% and 5.2% for trichomoniasis,6,14,15,32,34,35 and between 0% and 7.1% for C. trachomatis.4,6,14–16,32,34–36 The increased rates of trichomoniasis and chlamydial infection seen in this study could be a reflection of more frequent heterosexual experiences with male sexual partners within the past 12 months, the higher prevalence of these infections in racial minority groups in the southern United States,28,37 or due to issues regarding lack of healthcare insurance (67.4% of women in the study reported not having healthcare insurance) with subsequent underutilization of healthcare services, including HIV/STD screening services. Additionally, the use of T. vaginalis InPouch culture may also have contributed to the higher rates of trichomoniasis seen in this study compared with prior studies of WSW and WSWM, several of which only used wet preparation for diagnosis.14,32,34 The sensitivity of wet prep (standard practice at the MSDH STD clinic and other public health clinics across Mississippi) for diagnosis of trichomoniasis in this study (using InPouch culture as the gold standard) was 65.7%.

Also of interest is the fact that there was a greater difference in rates of C. trachomatis and N. gonorrhoeae infection between exclusive AAWSW and AAWSWM compared with rates of trichomoniasis and M. genitalium infection. One potential explanation for this finding may be that differential participation in types of sexual activities within sexual risk groups (WSW vs. WSWM) may account for differences in rates of transmission of these organisms. For example, women engaging in penile-vaginal sex with men would be more likely to acquire a greater inoculum of C. trachomatis and/or N. gonorrhoeae transmitted through seminal fluid than women engaging in digital-vaginal penetration or penetration with sex toys with other women, sexual activities that have an unknown risk for transmission of these organisms. In contrast, transmission of trichomoniasis between women has been documented,8,38 although the frequency of this event is not well known. Alternatively, this observation could result in part from differences in the duration of untreated infection between the 4 organisms and rates of new sexual partner acquisition. Further study of this issue in WSW compared with WSWM will be of considerable interest.

Also of note, 3 cases of C. trachomatis, 1 case of N. gonorrhoeae, and 5 cases of M. genitalium were diagnosed among women reporting no history of sex with men in the past 12 months. Additionally, 1 woman in this group, infected with both C. trachomatis and M. genitalium, denied lifetime history of sex with a male partner. It could be hypothesized that this woman acquired these STIs from another female sexual partner although this cannot be proven as sexual partner(s) were not available for testing. Prior reports of transmission of C. trachomatis and N. gonorrhoeae between WSW have largely been anecdotal and unpublished.22 As mentioned previously, little is known about the efficiency of transmission of these STIs between women. Exchange of infected cervicovaginal secretions during receptive vaginal and anal sexual activity with fingers, hands, and sex toys is the most plausible mechanism, as supported by reports of infection with genital human papillomavirus,12,19,20 HIV,10,11 and trichomoniasis8,38 among women reporting sexual activity exclusively with women. Further study of sexual partnerships among women exclusively having sex with other women in whom both partners are infected with C. trachomatis or N. gonorrhoeae should be conducted to gain further insight on this issue. Additionally, prior data does not exist on the prevalence of M. genitalium among WSW, and it is unknown if this pathogen can be sexually transmitted between women.

Few studies have looked at subpopulations of sexual minority women to examine the frequency of risk-taking behaviors that could facilitate STI acquisition or transmission. Findings from our study demonstrate that AAWSWM who have had a male sex partner within the past 12 months were significantly more likely than exclusive AAWSW to report engaging in behaviors that are known risk factors for STI infection (such as reporting a history of transactional sex and having sex with a homosexual or bisexual man during the past 12 months). They were significantly more likely to report history of chlamydia and gonorrhea infection, and be diagnosed with trichomoniasis, C. trachomatis, N. gonorrhoeae, or any STI than exclusive AAWSW. These heightened sexual risk-taking behaviors among WSWM have also been noted in data from a large British probability survey conducted between 1999 and 2001.39 This survey found that WSWM over the past year were significantly more likely to report greater numbers of male partners, anal intercourse, failure to use barrier protection, and alcohol and drug abuse than women reporting sex exclusively with men (WSM). WSWM also had an increased likelihood of induced abortion and STI diagnosis (age-adjusted odds ratios = 3.07 and 4.41, respectively) than WSM. Another study of sexual risk factors among self-identified lesbian, bisexual, and heterosexual women accessing primary care settings found that bisexual women reported substance use with sex at a higher rate than lesbians or heterosexual women (P < 0.001).40 Bisexual women also had more homosexual male partners and a higher mean number of male sexual partners than heterosexual women (P < 0.001). In addition, self-identified bisexual women have also been found to experience a higher likelihood of frequent mental distress (P < 0.001) and poorer general health (P < 0.01) than women identifying as lesbian.41 Overall, this growing body of data is beginning to show that WSWM may be a unique at-risk group of women that merits tailored STI/HIV intervention efforts.

As mentioned previously, 67.4% of AAWSW in our study reported not having health insurance. This lack of insurance with subsequent underutilization of health care services may have contributed to the high rates of trichomoniasis and chlamydial infection noted. This percentage of uninsured women is significantly higher than that noted in a recent Kaiser Family Foundation report compiling population-based data on health insurance status of American women by state and by race/ethnicity.42 In this Kaiser report, approximately 27.0% of all AA women living in Mississippi did not have health insurance. Identifying reasons that would explain this discrepancy in health insurance rates between AAWSW and the general population of AA women in Mississippi was beyond the scope of the current study. In addition, how this finding impacts utilization of healthcare services by AAWSW is unknown but merits further study.

Our study has several limitations. First, data were collected from a small (n = 196) convenience sample of AAWSW presenting to a large urban STD clinic, limiting the generalizability of the results to other populations of AAWSW. This limitation is inherent to many prior studies of WSW as this group is frequently a hidden population and difficult to access. Second, the small sample size limited our ability to include variables found to be significant in univariate analysis (such as marital status) in the multivariable analysis to look for independent associations. Third, the majority of the data collected in this study was obtained by participant self-report and was inherently limited by recollection bias or social desirability bias by the respondents. Fourth, as this was a pilot study and did not include participant compensation, the numbers of questions asked in the written questionnaire were limited. Consequently, we were unable to explore detailed sexual practices (oral, vaginal, and/or anal) that participants may engage in with their female and male sexual partners and assess which practices were more likely to be associated with diagnosis of an STI. Future studies of AAWSW and AAWSWM should attempt to include this information. Finally, the cross-sectional design of this study limits our ability to determine STI incidence, rates of reinfection, and changes in partnership dynamics over time among this group of women and how this may affect their STI rates. A prospective analysis of AAWSW, evaluating their sexual risk behaviors, changes in partnership gender and number over time, and STI incidence is an important next step in this line of research.

In conclusion, we are only just beginning to understand the burden of disease due to HIV/STI among AAWSW living in the southern United States. This is the first study that specifically focuses on this aspect of sexual health among this group of racial- and sexual-minority women. Prevalence of trichomoniasis, C. trachomatis, N. gonorrhoeae, and M. genitalium was high, comparable with heterosexual women receiving STI services in our STD clinic (data not shown). Recent sex with men was common, and independently predicted report of substance use within the past 30 days, history of gonorrhea infection, and a new diagnosis of trichomoniasis and chlamydial infection. AAWSWM, as a subgroup, may demonstrate heightened sexual risk-taking behaviors and higher STI rates compared with exclusive AAWSW. Sexual health services provided to AAWSW should take into account partner gender heterogeneity and all aspects of sexual orientation when screening for STI and providing prevention counseling.

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