Introduction

Because the risk of sexual transmission of HIV between women is assumed to be low if not nonexistent, lesbian women and other women who have sex with women (WSW) are generally not seen as vulnerable to HIV infection. Although a few case reports suggest the possibility of female to female transmission [1], [2], systematic evidence about the viability of this route of transmission is lacking [3]–[7]. The absence of such evidence has been attributed to a lack of attention for this mode of transmission, or the institutionalized exclusion of lesbian women from “risk group” categories [8], [9]. On many occasions and in several forums, lesbian activists have strongly objected to their omission and the de-prioritization of their risk for HIV transmission [10], [11]. This lack of attention might reinforce the myth of “lesbian immunity” [12]–[16], and the idea among lesbian women of not being at risk [13], [17], leaving them ill-equipped to protect themselves and their partners.

The accumulating evidence regarding the transmissible reproductive tract infections in lesbian women and other WSW warrants attention for HIV/AIDS among this population [18]. For instance, Singh and colleagues found an elevated prevalence of chlamydia trachomatis among WSW compared to women who reported sex with men only [19]. Studies furthermore have shown that human papillomavirus (HPV) is common among WSW, while evidence strongly suggests that HPV transmission occurs among WSW [20]–[22]. Finally, bacterial vaginosis (BV) in WSW was found to be associated with number of female sexual partners, but not with sex with men, suggesting that BV is sexually transmitted between women [23].

Despite the ongoing silence, the presence of HIV/AIDS in lesbian women and other WSW has been documented since the early 1990s, with prevalence rates that are sometimes higher than among their heterosexual counterparts [3], [15], [24]–[29]. This increased risk of HIV is usually associated with injection drug use and sexual involvement with men. For instance, Diaz et al. reported among female injection drug users a higher infection rate in WSW compared to exclusively heterosexual women; WSW were also more likely than heterosexual women to have had unprotected sex with an older male injection drug user [26]. That WSW more frequently engage in HIV risk practices is furthermore suggested by findings from a study in which WSW were compared with women who reported that they never had engaged in sexual interactions with other women. In this study WSW were more likely to report previous sexual contact with a homo−/bisexual man, or with an injection drug user [30]. Sexual contact with men seems to occur frequently among lesbian women and other WSW [31]–[33]: Diamant et al. reported, for instance, that in a sample of 6935 self-identified lesbians in the United States, over 77% had one or more lifetime male sexual partners, while close to 6% had a male sexual partner in the preceding year [34]. In the National Health and Nutrition Examination Surveys (NHANES), a series of cross-sectional surveys conducted by the National Center for Health Statistics to compile nationally representative statistics on the health of the US population, 9.6% and 84.4% of all women who identified as lesbian or homosexual had had sex with one or more men in the preceding year or during their life [31].

Most studies about lesbian women and other WSW and HIV/AIDS have focused on special populations, such as women who are HIV-positive and injection drug users (e.g. [35]–[37], and have been conducted in high income countries [37]. Studies of HIV/AIDS in general samples of WSW and WSW in middle and low income countries, some of which have the highest HIV prevalence worldwide, are rare [38]. In addition, HIV testing behavior in WSW has hardly been explored. To address this gap, we conducted a community-based survey among a sample of lesbian women and other WSW in Southern Africa to assess the prevalence of HIV-testing and HIV infection, and to identify the characteristics of women who reported to be HIV-positive among those that had been tested.

Materials and Methods

Results

In total, 591 women who met the eligibility criteria participated in the study (see Table 1 for a description of the sample). Most women lived in South Africa. Although the women’s ages ranged from 18 to 65, the sample was relatively young. Almost half of the women had completed secondary education or less; the other women had been or were still involved in some kind of higher level education. Most women identified their race as black; for analytic purpose we combined white (5.9%) and Asian/Indian (2.9%) women into the category “other”). About a third of the women were full-time employed and another third was unemployed. Almost half of the women reported to have a regular income. More than a third of the women were covered by some kind of health insurance.

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Table 1. Characteristics of Southern African WSW who have and who have not been tested for HIV.

https://doi.org/10.1371/journal.pone.0053552.t001

Almost one in every 10 women reported to currently being married or to have been married in the past. About a quarter of the women reported to be the biological parent of children. While most women reported to be in an ongoing intimate relationship, a third was currently living with the intimate partner. The majority of women said they were only sexually attracted to women and identified as lesbian or gay. Almost half of the women reported to ever have had consensual sex with a man; almost 1 in 5 women had consensual sex with a man in the preceding year. Transactional sex with men was reported by 10.5% of the women and transactional sex with women was reported by 15.2% of the women; ‘money’ was the most frequently reported reason for transactional sex with men as well as with women. Forced sex by men (lifetime) was reported by a quarter of the women and lifetime forced sex by women was reported by one of every 6 women. The (lifetime) use of any recreational drug was reported by half of all women (the most frequently reported drug was marijuana; use of any other drugs was only reported by small groups of women); a very small proportion of women reported to have used a needle to inject drugs into their body for other than medical reasons.

Most of the women in the sample had ever been tested for HIV (78.3%). Women who reported to have ever been tested for HIV were older (see Table 1), less likely to be a student or unemployed compared to being full-time employed, more likely to have a regular income and have health insurance Compared to women from South Africa, women from Botswana were more likely to have been tested. Women who were a biological parent were also more likely to have been tested. In terms of gender and sexual orientation and actual sexual behavior, we found that women who perceived themselves as more masculine were less likely to have been tested, while women who perceived themselves as relatively more feminine were more likely to have been tested. Compared to women who only had one female sexual partner (lifetime), women with 2 to 4 partners and 5 to 9 were more likely to ever have been tested. Compared to women who never had any male sexual partners, women who had had one male sexual partner or 2 or more partners were more likely to have been tested. Finally, women who had engaged in transactional sex with women only (lifetime) were less likely to have been tested compared to women who never engaged in transactional sex.

Women who had never been tested for HIV were asked to indicate the main reason for not having been tested. As shown in Table 2, the two reasons endorsed most frequently seem to be in contrast with each other. A majority of untested women indicated that they had not been tested out fear of finding out the test results. At the same time, 39.0% of the untested women indicated that they think that they are not at risk. Other reasons were mentioned less frequently. Still, 12.2% of the untested women mentioned potential discrimination and 6.5% of the women mentioned potential embarassment as a reason for not having been tested. Practical barriers such as costs of the test and not knowing where to go were rarely mentioned.

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Table 2. Reasons for not getting tested for HIV among untested women (n = 128).

https://doi.org/10.1371/journal.pone.0053552.t002

In the multivariate analysis, none of the demographic and sexual and gender orientation variables were significantly associated with ever having been tested for HIV (Table 2). The factors still associated with having been tested related to the women’s sexual behavior. Compared to women who only had one female sexual partner (lifetime), women with 2 to 4 and 5 to 9 partners were more likely to ever have been tested. Compared to women who never had any male sexual partners, women who had had 2 or more partners were more likely to have been tested. Women who reported ever engaging in transactional sex with women only or with both women and men were less likely to have been tested compared to women who never engaged in transactional sex.

Thirty-four (7.3%) of the 463 women who had been tested for HIV reported not to know their serostatus. Of the 429 women who knew their serostatus, 41 women (9.6%; 6.9% of the sample including the women who had never been tested for HIV or who did not know their serostatus) reported to be HIV-positive. Bivariately, women living with HIV/AIDS were more likely to be older, to be married or have been married, and to be a biological parent than women who tested negative (see Table 3). In terms of sexual orientation and gender identification, lesbian women living with HIV/AIDS were more likely to only be attracted to women (rather than to both women and men), and to see themselves comparatively as less feminine.

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Table 3. Characteristics of Southern African WSW who tested negative or positive for HIV.

https://doi.org/10.1371/journal.pone.0053552.t003

In terms of behavioral risk factors, neither the number of female partners, nor the number of male partners was associated with being HIV-positive. Compared to women who never engaged in transactional sex, women who during their lifetime had had transactional sex with both men and women were more likely to be HIV-positive. Compared to women who did not report any forced sexual experiences, women who had had forced sex only by men, only by women, or by both men and women, were more likely to be HIV-positive. Lifetime drug use, recreational or intravenous, did not increase the odds of being HIV-positive.

In the multivariate analysis, none of the demographic and sexual and gender orientation variables were anymore associated with HIV serostatus except for age: lesbian women living with HIV/AIDS were likely to be older. Having engaged in transactional sex was also no longer associated with HIV serostatus. The only factor still associated with living with HIV was ever having had forced sexual experiences. Compared to women who did not report any lifetime forced sexual experiences, women who had had forced sex only by men, only by women, or by both men and women, were more likely to report being HIV-positive. To check whether our findings were affected by the absence of any HIV positive women in Botswana, we ran all analyses excluding the women from Botswana. This did not seem to affect the outcomes: age and forced sex experiences only by men, only by women, and by both men and women were all associated with self-reported positive HIV status.

In trying to identify the most likely transmission route for the 41 women who were HIV-positive, we found that 2 of them reported to ever have used needles for intravenous drug use. Twenty-six women reported to ever have had consensual sex with and/or forced sex by men. Based on the available data we could not identify a transmission route for 13 of the infected women.

Discussion

The majority of lesbian women and other women who have sex with women in this sample had tested for HIV at least once. Indicators of sexual risk were sometimes positively and at other times negatively related to having been tested. For instance, women were more likely to have been tested if they had had sex with men, but they were less likely to have been tested if they had engaged in transactional sex with men and women; some of the HIV testing could have taken place in the context of prenatal care. As in studies among South African MSM [40], not having tested for HIV also seemed an indication of social vulnerability: unemployed women, women without regular income and health insurance, and gender non-conforming women were less likely to have been tested. The fact that fear of finding out HIV test results was the most frequently endorsed reason among the women who had not been tested suggests that there is an awareness of the possibility that one might be infected. We were not able to assess the validity of the second reason that was most frequently endorsed: the perception of not being at risk.

About one in ten of the women who knew their HIV status reported to be living with HIV. From the perspective that lesbian women are invulnerable to HIV, this prevalence would seem high. At the same time, it is lower than the general HIV prevalence in each of the four countries [41]. The observed prevalence of 9.6% could be an underestimate, because the serostatus that women reported was not necessarily recent and because the HIV prevalence among the untested women could have been higher than among the tested women. Surprisingly, the only factor that was independently associated with a self-reported positive HIV status among the tested women was having had forced sex, not just by men but also by women. Because of the study’s cross-sectional design, it is not possible to determine whether the forced sex experiences preceded the infection or whether they were the actual cause of the infection. It is likely, that forced sex is associated with other factors that increase women’s risk. Various studies have shown that WSW not only have more health risk factors and lower levels of protective factors compared to non-WSW [32], [36], [42], but that health risk factors also tend to cluster. Lewis [43] for instance found how substance use, interpersonal violence, and discrimination tend to co-occur among women who have sex with women.

In terms of the source of infection, we could not identify the most likely transmission route of about a third of the women. We cannot rule out that these women were infected at birth or through medical procedures. It is, however, also possible that these women were infected in sexual interactions with other women.

The study findings should be seen in the context of some study limitations. First, the sample studied is a convenience sample; it is likely that women who were more comfortable with their same-sex sexuality and better connected to other women who have sex with women were more likely to participate. Based on the judgments of the community-based organizations, younger women, black women, and women living in urban areas were likely to be overrepresented. It is not clear how this affected the reported findings. Furthermore, all findings, including HIV status, are based on self-report. Although studies showed that self-reports of HIV test results are reliable [44]–[46], we cannot exclude the possibility that some women, for instance women with forced sex experiences, were more likely to think they were HIV positive than women without such experiences. Another limitation is that the questionnaire was only offered in an English version. It is likely that this restricted participation of women with little command of English and it might have caused some problems in filling out the questionnaires.

Our findings make clear that HIV affects Southern African lesbian, bisexual and other women who have sex with women. This should have several implications for HIV prevention and health care, and HIV/AIDS policies more generally. Most importantly, our data make clear, as other studies have done before [31]–[34], [47], that sexual identification as ‘lesbian’ does not exclude any sexual involvement with men, both on a lifetime basis as well as more recently. This implies that prevention messages about HIV risk should be made relevant for WSW in order for them to feel included and addressed. Furthermore, reporting of same-sex sexuality should not deter health care providers from addressing sexual risk [34], [48], while health care providers should be capacitated to provide non-judgmental care to WSW, who usually experience formidable barriers to access critical preventive health care and treatment services [49]. In general, in the Southern African context, HIV/AIDS policy should also address the needs of lesbian, bisexual and other women who have sex with women. This will be most effective if the heterogeneity of the population of WSW is recognized and programs are tailored in such a way that they best suit the needs of WSW locally.

Our findings furthermore suggest the need for research that addresses WSW’s awareness of HIV and STI risk and their engagement in sexual risk practices; few studies [12], [50] have done so thus far, while some studies have shown that adoption of safer sex practices among WSW is rare (e.g., [51]). In addition, we need to understand how accurate, appropriate and complete counseling could be provided to WSW living with HIV in order to prevent transmission to other female sex partners. Furthermore, our findings suggest a need to better understand forced sexual experiences of WSW with both men and women and their consequences for health behaviors and general health.

Supporting Information

Acknowledgments

This research project was designed and implemented in collaboration with the following community organizations: Behind the Mask, South Africa, Durban Lesbian and Gay Community & Health Centre, South Africa; Forum for the Empowerment of Women, South Africa; Gays and Lesbians of Zimbabwe, Zimbabwe; LeGaBiBo (Lesbians, Gays and Bisexuals of Botswana), Botswana; OUT LGBT Well-Being, South Africa; Out-Right Namibia; and Triangle Project, South Africa. We thank all study participants and the Southern African Lesbian and Bisexual Women Research Team for their contribution to the project.