Abstract
Compared to Black cisgender MSM, Black transgender women had a higher incidence of bacterial sexually transmitted infections (25.9 [11.1–46.3] vs 9.6 [8.10–11.3] per 100 person-years), higher rates of income and housing insecurity, and condomless receptive anal intercourse. Further investigation of unique risk pathways among transgender women is critical.
Brief Summary:
We report differing correlates of incident STI among Black cisgender men who have sex with men compared to Black transgender women, noting higher incidence overall among transgender women.
Introduction
Cisgender men who have sex with men (MSM) and transgender women (TGW) are at particular risk for bacterial sexually transmitted infections (BSTI) (1, 2). MSM and TGW, however, constitute two different populations, and research conflating the two groups runs the risk of undermining unique differences between them and divergent prevention and treatment strategies optimally suited for each (3, 4). In 2014 the World Health Organization called for the inclusion of TGW as a distinct population in the global response to HIV (5), yet the understanding of the differences in HIV and BSTI risk between MSM and TGW remains incomplete. Elucidation of the drivers of BSTI unique to TGW may facilitate more targeted prevention efforts. We aimed to evaluate BSTI risk factors separately among Black MSM and TGW participating in the HIV Prevention Trials Network (HPTN) 061 study (6, 7).
Methods
HPTN 061 assessed the feasibility of a multi-component intervention to reduce HIV infection among Black MSM (6, 7) in Atlanta, Boston, Los Angeles, San Francisco, Washington DC, and New York between July 2009 and October 2010 (8). Testing for HIV and urogenital and rectal BSTI were performed at baseline, 6, and 12 months. Eligibility was defined as individuals ≥18 years of age, self-identifying as male at birth, as well as Black, African American, Caribbean Black, or multiracial Black, and that they were either HIV-negative or living with HIV but not engaged in care. Gender identity was based on self-identification, with TGW defined as individuals endorsing any one or more of the following genders: female (n=5), transgender (n=19), transsexual (n=6), genderqueer (n=3), realness (n=2), butch queen (n=1), femme queen (n=3), intersex (n=2), or crossdresser (n=2).
BSTI testing was done using nucleic acid amplification testing with the Gene-Probe Aptima Combo 2 assay (Hologic, San Diego, CA) for Neisseria gonorrhoeae and Chlamydia trachomatis, while rapid plasma reagin (RPR) and confirmatory treponemal antibody testing was performed for Treponema pallidum. A diagnosis of syphilis was defined as a newly reactive RPR with a positive confirmatory treponemal test or a four-fold increase in RPR titers after appropriate earlier treatment. A standardized questionnaire via audio computer-assisted self-interview was administered to each participant to capture sociodemographic and behavioral characteristics.
The primary outcome was first incident BSTI at any anatomic site over the 12-month follow-up period, among those with completed follow-up, excluding baseline BSTI. Individuals with a BSTI at any point received prompt therapy, as did those with HIV infection who had not previously been linked to care. We calculated the incidence and 95% confidence intervals (CIs) of first BSTI separately for cisgender MSM and TGW overall and by each covariate. We compared, descriptively, risk differences in BSTI by each covariate between cisgender MSM and TGW. All analyses were conducted using STATA 16.0 (StataCorp, College Station, TX). All participating institutions provided institutional review board approval.
Results
Overall, 1,374 individuals were followed for the entire 12-month study period, 1,347 (98.0%) of whom identified as cisgender MSM, while 27 (2.0%) were classified as TGW. Twelve-month retention was 87.1% (27/31) for TGW and 88.5% (1,347/1,522) for MSM (p=0.8). The incidence of BSTI was 9.6 per 100 person-years (95% CI 8.1–11.3) and 25.9 per 100 person-years (95% CI 11.1–46.3) among cisgender MSM and TGW, respectively (p=0.008).
MSM who identified as straight had 10 fewer BSTI per 100 person-years than MSM who did not identify as straight, while straight identification among TGW was associated with 15 more BSTI per 100 person-years compared to non-straight TGW (Table). There were 9 fewer BSTI per 100 person-years among TGW with greater than high school education compared to high school or less; there was no difference in BSTI risk by educational attainment among MSM. While incidence of BSTI among cisgender MSM did not differ between those with and without healthcare coverage, among TGW, healthcare coverage was associated with 18 fewer BSTI per 100 person-years than among TGW without healthcare coverage. A new diagnosis of HIV compared to testing negative, reporting a new anal sex partner, using saliva as lubricant, and receiving money or drugs for sex were all associated with higher rates of BSTI among both cisgender MSM and TGW. Baseline BSTI compared to no baseline BSTI, and condomless receptive anal sex compared to no receptive anal intercourse was associated with larger risk differences among TGW than among cisgender MSM. Among TGW, but not among cisgender MSM, current membership in a religious institution was associated with 48 fewer BSTI per 100 person-years compared to not being a member of a religious institution.
Table:
Baseline characteristics associated with incident bacterial STI among cisgender MSM and transgender women from 6 U.S. Cities, 2009–2011
| Cisgender men who have sex with men | Transgender women who have sex with men | |||||||
|---|---|---|---|---|---|---|---|---|
| Incident STI diagnoses | Person-years | STI incidence per 100 person years (95%CI) | Risk difference per 100 person years (95%CI) | Incident STI diagnoses | Person-years | STI incidence per 100 person years (95%CI) | Risk difference per 100 person years (95%CI) | |
| Socio-demographic characteristics | ||||||||
| Overall | 130 | 1347 | 9.6 (8.1, 11.3) | 7 | 27 | 25.9 (11.1, 46.3) | ||
| Age at enrollment, years | ||||||||
| 18–29 | 82 | 434 | 18.9 (15.2, 22.6) | REF | 5 | 12 | 41.7 (13.2, 70.1) | REF |
| 30 and elder | 50 | 929 | 5.4 (3.8, 6.7) | −13.6 (−17.6, −9.7) | 2 | 15 | 13.3 (1.7, 40.4) | −28.3 (−61.7, 5.1) |
| Sexual orientation | ||||||||
| Gay, queer, same gender loving, another sexual orientation | 110 | 905 | 12.2 (10.0, 14.3) | REF | 5 | 20 | 25.0 (8.7, 49.1) | REF |
| Bisexual | 19 | 386 | 4.9 (3.0, 6.8) | −7.3 (−10.1, −4.5) | 0 | 2 | 0 | Not estimated |
| Straight | 1 | 56 | 1.8 (0.3, 3.4) | −10.3 (−13.1, −7.4) | 2 | 5 | 40.0 (5.3, 85.3) | 15.0 (−33.0, 63.0) |
| Ethnicity | ||||||||
| Non-Hispanic | 123 | 1254 | 9.8 (8.2, 11.5) | REF | 7 | 23 | 30.4 (13.2, 52.9) | REF |
| Hispanic | 7 | 93 | 7.5 (0.22, 12.9) | −2.3 (−7.9, 3.3) | 0 | 4 | 0 | Not estimated |
| Race | ||||||||
| Black/African American | 118 | 1268 | 9.3 (7.8, 10.9) | REF | 6 | 25 | 24.0 (9.3, 45.2) | REF |
| Multiracial | 12 | 79 | 15.2 (7.3, 23.1) | −5.9 (−2.2, 14.0) | 1 | 2 | 50.0 (1.3, 98.7) | 26.0 (−46.6, 98.6) |
| Relationship status | ||||||||
| Legal partnership/main partner | 18 | 143 | 12.6 (7.1, 18.0) | REF | 2 | 7 | 28.6 (3.7, 71.0) | REF |
| Single/divorced/widowed | 112 | 1204 | 9.3 (7.7, 10.9) | −3.3 (−2.4, 9.0) | 5 | 20 | 25.0 (8.7, 49.1) | 3.6 (−35.6, 42.8) |
| Highest level of education | ||||||||
| High school or less | 65 | 699 | 9.3 (7.1, 11.4) | REF | 5 | 21 | 23.8 (8.2, 47.2) | REF |
| Greater than high school | 65 | 647 | 10.0 (7.7, 12.4) | 0.7 (−2.0, 3.4) | 2 | 6 | 33.3 (4.3, 77.7) | 9.5 (−33.2, 52.2) |
| Housing | ||||||||
| Homeless, shelter, transitional housing | 8 | 181 | 4.4 (1.4, 7.4) | REF | 2 | 10 | 20.0 (2.5, 55.6) | REF |
| Lives alone, with partner, with family, with friends | 122 | 1166 | 10.5 (8.7, 12.2) | 6.0 (2.6, 9.5) | 5 | 17 | 29.4 (10.3, 56.0) | 9.4 (−24.1, 43.0) |
| Income, per year | ||||||||
| Less than $20,000 | 63 | 787 | 8.0 (6.1, 9.9) | REF | 3 | 17 | 17.6 (3.8, 43.4) | REF |
| $20,000 or greater | 66 | 547 | 12.1 (9.3, 14.8) | 4.1 (0.7, 7.4) | 4 | 9 | 44.4 (13.7, 78.8) | 26.8 (−11.1, 64.7) |
| Healthcare coverage | ||||||||
| No | 58 | 568 | 10.2 (7.7, 12.7) | REF | 4 | 11 | 36.3 (10.9, 69.2) | REF |
| Yes | 72 | 779 | 9.2 (7.2, 11.3) | 1.0 (−4.2, 2.2) | 3 | 16 | 18.7 (4.0, 45.6) | −17.6 (−52.5, 17.3) |
| Ever incarcerated | ||||||||
| No | 65 | 548 | 11.9 (9.1, 14.6) | REF | 3 | 7 | 42.9 (9.9, 81.6) | REF |
| Yes | 65 | 796 | 8.2 (6.3, 10.1) | −3.7 (−7.0, −0.04) | 4 | 20 | 20.0 (5.7, 43.7) | −22.9 (−64.3, 18.6) |
| Study site | ||||||||
| Boston, MA | 6 | 156 | 3.8 (0.8, 6.9) | REF | 0 | 2 | ||
| Georgia | 32 | 276 | 11.6 (7.8, 15.4) | 7.7 (2.9, 12.6) | 1 | 3 | ||
| Los Angeles, CA | 24 | 249 | 9.6 (6.0, 13.3) | 5.8 (1.0, 10.5) | 1 | 3 | 10.5 (1.3, 33.1) | REF |
| New York, NY | 22 | 281 | 7.8 (4.7, 11.0) | 4.0 (−0.4, 8.4) | 0 | 4 | ||
| San Francisco, CA | 5 | 187 | 2.7 (0.4, 5.0) | −1.2 (−5.0, 2.6) | 0 | 7 | ||
| Washington, DC | 41 | 198 | 20.7 (15.1, 26.3) | 16.9 (10.5, 23.3) | 5 | 8 | 62.5 (24.5, 91.5) | 52.0 (15.0, 88.9) |
| Clinical characteristics | ||||||||
| HIV status | ||||||||
| Previously diagnosed HIV | 13 | 153 | 8.5 (4.1, 12.9) | 0.3 (−4.0, 5.0) | 2 | 4 | 50.0 (6.7, 93.2) | 29.0 (−24.4, 82.3) |
| New HIV diagnosis | 27 | 124 | 21.8 (14.5, 29.0) | 13.6 (6.1, 21.0) | 1 | 3 | 33.3 (0.8, 90.6) | 12.3 (−45.2, 69.8) |
| HIV-negative | 86 | 1047 | 8.2 (6.5, 9.9) | REF | 4 | 19 | 21.0 (6.0, 45.6) | REF |
| Unknown | 4 | 23 | 17.4 (1.9, 32.9) | 9.2 (−6.4, 24.8) | 0 | 1 | Not estimated | Not estimated |
| Any bacterial STI at baseline | ||||||||
| No | 83 | 1172 | 7.1 (5.6, 8.5) | REF | 5 | 24 | 20.8 (7.1, 42.1) | REF |
| Yes | 47 | 175 | 26.9 (20.3, 33.4) | 19.8 (13.0, 26.5) | 2 | 3 | 66.7 (9.4, 99.2) | 45.8 (−11.0, 102.7) |
| Behavioral characteristics during follow-up | ||||||||
| New anal sex partners, prior 6 months | ||||||||
| No | 24 | 525 | 4.6 (2.8, 6.4) | REF | 1 | 7 | 14.3 (0.4, 57.9) | REF |
| Yes | 106 | 822 | 12.9 (10.6, 15.2) | 8.3 (5.4, 11.2) | 6 | 20 | 30.0 (11.9, 54.3) | 15.7 (−17.7, 49.1) |
| Receptive anal sex, prior 6 months | ||||||||
| No receptive anal sex | 34 | 543 | 6.3 (4.2, 8.3) | REF | 1 | 2 | 50.0 (1.3, 98.7) | REF |
| Always used condoms during receptive anal sex | 13 | 105 | 12.4 (6.1, 18.7) | 6.1 (−0.5, 12.7) | 1 | 2 | 50.0 (1.3, 98.7) | 0 (−99.9, 99.9) |
| Condomless receptive anal sex | 83 | 699 | 11.9 (9.5, 14.3) | 5.6 (2.5, 8.8) | 5 | 23 | 21.7 (7.5, 43.7) | −28.3 (−101.0, 44.4) |
| Insertive anal sex, prior 6 months | ||||||||
| No insertive anal sex | 24 | 182 | 13.2 (8.3, 18.1) | REF | 4 | 10 | 40.0 (12.2, 73.8) | REF |
| Always used condoms during insertive anal sex | 11 | 124 | 8.9 (3.9, 13.9) | −4.3 (−11.3, 2.7) | 0 | 1 | 0 | Not estimated |
| Condomless insertive anal sex | 95 | 1041 | 9.1 (7.4, 10.9) | −4.1 (−9.3, 1.2) | 3 | 16 | 18.8 (4.0, 45.6) | −21.2 (−57.8, 15.3) |
| Saliva as lubricant during anal sex, prior 6 months | ||||||||
| No | 91 | 1096 | 8.3 (6.7, 9.9) | REF | 5 | 21 | 23.8 (8.2, 47.2) | REF |
| Yes | 39 | 251 | 15.5 (11.0, 20.0) | 7.2 (2.5, 12.0) | 2 | 6 | 33.3 (4.3, 77.7) | 9.5 (−33.2, 52.2) |
| Travel for sex, prior 6 months | ||||||||
| No | 72 | 993 | 7.3 (5.6, 8.9) | REF | 6 | 17 | 35.3 (14.2, 61.7) | REF |
| Yes | 58 | 354 | 16.4 (12.5, 20.2) | 9.1 (5.0, 13.3) | 1 | 10 | 10.0 (0.2, 44.5) | −25.3 (−55.2, 4.6) |
| Received drugs or money, prior 6 months | ||||||||
| No | 7 | 294 | 2.4 (0.6, 4.1) | REF | 1 | 6 | 16.7 (0.4, 64.1) | REF |
| Yes | 123 | 1053 | 11.7 (9.7, 13.6) | 9.3 (6.7, 11.9) | 6 | 21 | 28.6 (11.3, 52.2) | 11.9 (−24.3, 48.1) |
| Substance use, prior 6 months | ||||||||
| Methamphetamine | ||||||||
| No | 123 | 1129 | 3.2 (0.9, 5.5) | REF | 6 | 25 | 24.0 (9.3, 45.1) | REF |
| Yes | 7 | 218 | 10.9 (9.1, 12.7) | 7.7 (4.7, 10.6) | 1 | 2 | 50.0 (1.3, 98.7) | 26.0 (−46.6, 98.6) |
| Poppers | ||||||||
| No | 116 | 1115 | 6.0 (3.0, 9.1) | REF | 7 | 26 | 26.9 (11.6, 47.8) | REF |
| Yes | 14 | 232 | 10.4 (8.6, 12.2) | 4.4 (0.8, 7.9) | 0 | 1 | 0 | Not estimated |
| Erectile dysfunction medications | ||||||||
| No | 126 | 1140 | 1.9 (0.06, 3.8) | REF | 7 | 26 | 26.9 (11.6, 47.8) | REF |
| Yes | 4 | 207 | 11. 1 (9.2, 12.9) | 9.2 (6.5, 11.7) | 0 | 1 | 0 | Not estimated |
| Psychosocial measures at baseline | ||||||||
| Any intimate partner violence † | ||||||||
| No | 21 | 309 | 6.8 (4.0, 9.6) | REF | 1 | 2 | 50.0 (1.3, 98.7) | REF |
| Yes | 107 | 1007 | 10.6 (8.7, 12.5) | 3.8 (0.4, 7.2) | 5 | 24 | 20.8 (7.1, 42.1) | −29.2 (−101.7, 43.4) |
| Internalized homophobia * | ||||||||
| Low (7–16) | 75 | 614 | 12.2 (9.6, 14.8) | REF | 6 | 18 | 33.3 (13.3, 59.0) | REF |
| Medium (17–26) and High (27–35) | 50 | 688 | 7.3 (5.3, 9.2) | −4.9 (−8.2, −1.7) | 0 | 8 | 0 | Not estimated |
| CES-D score § | ||||||||
| < 16 | 47 | 459 | 10.2 (7.5, 13.0) | REF | 0 | 3 | 0 | REF |
| ≥ 16 | 76 | 745 | 10.2 (8.0, 12.4) | −0.04 (−3.6, 3.5) | 6 | 21 | 28.6 (11.3, 52.2) | Not estimated |
| Member of religious institution currently | ||||||||
| No | 50 | 565 | 8.8 (6.5, 11.1) | REF | 6 | 11 | 54.5 (23.4, 83.2) | REF |
| Yes | 80 | 778 | 10.3 (8.1, 12.4) | 1.4 (−1.7, 4.6) | 1 | 16 | 6.2 (0.2, 30.2) | −48.3 (−80.6, −16.0) |
| Member of religious institution growing up | ||||||||
| No | 27 | 340 | 7.9 (5.1, 10.8) | REF | 3 | 7 | 42.9 (9.9, 81.6) | REF |
| Yes | 102 | 1005 | 10.1 (8.3, 12.0) | 2.2 (−1.2, 5.6) | 4 | 20 | 20.0 (5.7, 43.7) | −22.9 (−64.3, 18.6) |
Co-variates were assessed through a computer-assisted self-interview (ACASI).
Any intimate partner violence includes psychological, physical and sexual violence at the hands of an intimate partner
Internalized homophobia was assessed via a self-measured scale adapted by Herek et al. (28).
CES-D is the 20-item Center for Epidemiologic Studies Depression Scale; a score of 16 or greater is associated with an increased risk for clinical depression (29).
Cisgender MSM reported higher levels of education and internalized homophobia and were more likely to report condomless insertive anal sex compared to TGW (Supplemental Table), while TGW were more likely to report housing and income insecurity, exchange sex, condomless receptive anal sex, and greater depression scores compared to cisgender MSM (p<0.01 for all comparisions).
Discussion
In light of recent concerns about prior studies that grouped TGW with cisgender MSM (9), we evaluated factors associated with BSTI among Black cisgender MSM and TGW separately, participating in HPTN 061. We found that identifying as straight, lower educational attainment, and lack of healthcare coverage were associated with increased risks differences for BSTI among TGW, but not among cisgender MSM, while condomless receptive anal intercourse and having a baseline BSTI were associated with higher risk differences among TGW than among cisgender MSM.
Those factors may reflect both structural and social barriers to accessing preventive services among a marginalized group, also reflected in the high rates of housing and income insecurity among TGW in our sample. Recent work has highlighted similar differences between TGW and MSM with regards to sexual risk behaviors (e.g., sex work and condom use) (9, 10), sexual partner identification methods (11), educational attainment (9), and financial security (12). Further, sexual networks among TGW are often less stable and more heterogeneous than among cisgender MSM (13). TGW also face higher rates of employment discrimination and marginalization (12, 14), which may contribute to higher rates of sex work (15). Some vulnerabilities experienced by TGW are more similar to those experienced by cisgender women than cisgender MSM including intimate partner violence, despite the mode of HIV acquisition being more similar among MSM and TGW (16). Further, a paradigm of conceptualizing sexual health risk in the context of a desire for gender affirmation has been outlined as a unique set of psychosocial and behavioral factors among TGW (17), and which may be modulated by distinct social networks (18).
Report of religious affiliation provided a protective effect against BSTI among TGW, substantiated by prior work in other populations (19, 20). Such findings may be attributable to affirming messages received by individuals who endorsed being a part of a religious institutions, supporting them in negotiating sexual risk taking (21). Whereas those unaffiliated with religious institutions may experience alienation from those institutions and internalized homophobia, which could lead to depression, substance use, and lower self-efficacy (21).
Notably, HPTN 061 enrollment was permissive of non-cisgender gender identities, thus recruitment efforts were not tailored in a culturally optimized manner towards TGW, resulting in their low levels of participation. That finding posed a limitation of this research, but has been echoed by many reports (22). TGW face numerous barriers to participation in trials and access to healthcare, including mistrust, lack of awareness, and fear of being “outed” (23). For health outcomes to be improved among TGW, a nuanced understanding of their specific risk pathways and development of culturally sensitive outreach and educational approaches will be essential, such as leveraging of peer-networks (24).
In summary, our results may be viewed as a call to action. Much more work is needed to delineate unique differences in BSTI risk among TGW in order to inform culturally appropriate interventions. Active recruitment of at-risk people with transgender identities should be a priority in the design of future studies; as an example, HPTN 083 has established a minimum recruitment number of TGW (25). Further, research into the benefits of culturally tailored care may reveal distinct treatment and prevention strategies beneficial for TGW, such as HPTN 091, currently enrolling TGW into a program that combines access to pre-exposure prophylaxis with gender-affirming care (26).
Limitations
Our study was limited by the low enrollment of TGW, reducing power and precision, but also making an analysis controlling for confounding not possible. We also lacked data on some confounding variables including participant use of peer-navigators, an important component of HPTN 061. Classification of TGW in our study was heterogeneous, and likely included nonbinary individuals; however, the transgender women enrolled in HPTN 061 had high levels of syndemic conditions associated with HIV risks seen in other studies of TGW at risk for HIV (e.g., poverty, experienced violence/victimization, depression, and substance use) (27). Although formal comparisons to other TGW are not appropriate, the comparable prevalence of risk factors suggests that the findings should be generalizable to other populations. Those limitations constitute an important reminder of the unique challenges faced in reaching TGW.
Conclusion
The incidence and drivers of BSTI differ among TGW and cisgender MSM. Much more work is needed to understand the unique STI prevention needs of TGW.
Supplementary Material
Conflicts of Interest and Sources of Funding:
HPTN 061 was supported by the National Institute of Allergy and Infectious Disease (NIAID), National Institute on Drug Abuse (NIDA) and National Institute of Mental Health (NIMH): Cooperative Agreements UM1 AI068619, UM1 AI068617, and UM1 AI068613. The work is partially supported by the Bio-behavioral and Community Science Core of the Harvard Center for AIDS Research (NIAID P30AI060354). Kenneth Mayer has received unrestricted research grants to study antiretrovirals for prevention from Gilead Sciences and Merck, Inc. The remaining authors have nothing to disclose. This manuscript is a product of authors and has not been reviewed by and does not necessarily represent the views of the HPTN or the study sponsors/funders.
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