Abstract
Purpose of Review
Pre-exposure prophylaxis (PrEP) represents one of the most effective methods of prevention for HIV, but remains inequitable, leaving many transgender and nonbinary (trans) individuals unable to benefit from this resource. Deploying community-engaged PrEP implementation strategies for trans populations will be crucial for ending the HIV epidemic.
Recent Findings
While most PrEP studies have progressed in addressing pertinent research questions about gender-affirming care and PrEP at the biomedical and clinical levels, research on how to best implement gender-affirming PrEP systems at the social, community, and structural levels remains outstanding.
Summary
The science of community-engaged implementation to build gender-affirming PrEP systems must be more fully developed. Most published PrEP studies with trans people report on outcomes rather than processes, leaving out important lessons learned about how to design, integrate, and implement PrEP in tandem with gender-affirming care. The expertise of trans scientists, stakeholders, and trans-led community organizations is essential to building gender-affirming PrEP systems.
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Designing gender-affirming PrEP systems goes beyond simply integrating gender-affirming care and PrEP services – it starts with partnerships with transgender scientists, stakeholders, trans-led community organizations, and community members at large.
Introduction
A decade after Truvada as oral HIV pre-exposure prophylaxis (PrEP, tenofovir disoproxil/emtricitabine) was approved in 2012 by the U.S. Food and Drug Administration (FDA) for public use [1], multiple interventions and programs have demonstrated PrEP’s effectiveness to curb HIV incidence. Since then, three new major advancements were made in PrEP formulation and delivery. In particular, the Descovy formulation of PrEP (emtricitabine/tenofovir alafenamide) was evaluated for safety and efficacy in 2019. It received FDA approval and provided a second oral PrEP option for some adults and adolescents, but importantly, people assigned female at birth were excluded from the clinical research on Descovy, resulting in the FDA’s limited approval of Descovy for people assigned male at birth only [2]. More recently approved in 2021, Apretude (cabotegravir extended-release injectable suspension) became the first long-acting injectable (LAI) option that makes it possible to take PrEP every 2 months instead of in a daily pill form, but again, this option has transgender-specific limitations, as transmasculine people were not included in the clinical trials [3]. Lastly, as an alternative to daily oral PrEP, “on-demand” or 2–1-1 PrEP, which follows an arranged schedule of taking two Truvada pills 2 to 24 ho before sex, one pill 24 h after the first dose, and another pill 24 h after the second dose, is currently endorsed by the Centers for Disease Control and Prevention (CDC) to be taken only when “at-risk” for HIV [4], and with studies demonstrating its efficacy and effectiveness, yet largely conducted in cisgender populations [5,6,7]. These are monumental and promising advances in the HIV prevention landscape and the broader mission to improve the health of communities and end HIV/AIDS around the world. However, their reach is limited among communities of transgender and nonbinary (trans) people, due to the ongoing underrepresentation of these communities in PrEP research and implementation globally.
Trans populations are diverse and include communities of transfeminine, transmasculine, and nonbinary individuals [8, 9••].Footnote 1 Trans communities face ubiquitous stigma, cissexism, and discrimination across all socio-ecological domains, including persistent structural efforts to delegitimize their gender identities and rights to access care, in addition to a dearth of comprehensive gender-affirming providers and services [10, 11]. These social and structural vulnerabilities place transgender and nonbinary communities at elevated risk for adverse behavioral and health outcomes, which further perpetuate to HIV inequities in this population [9••]. One recent study reported that transfeminine individuals, particularly those in the USA, have an estimated HIV prevalence of 14.1% [12••]. While existing data are scarce as a result of gender-blind surveillance systems [13], the limited data on transmasculine and nonbinary individuals who have sex with men show alarmingly high HIV incidence and prevalence as well [12••, 14]. Notably, the inequity in HIV prevalence is even more pronounced among minoritized ethnoracial groups [12••], within the trans community with estimates for HIV prevalence among Black, Indigenous, and Latine transgender women being substantially high [12••]. And community-led advocacy, research, and structural interventions that aim to promote HIV prevention interventions, including PrEP use, adherence, and persistence, must recognize the pressing need for equitable and transformative HIV prevention strategies that are rooted in and led by transgender and nonbinary communities [15,16,17,18].
Inequities in Designing PrEP Studies with Trans Populations
Despite a wide diversity of gender identities and expression, PrEP research has largely focused on transfeminine adults. While this focus on transfeminine adults is likely due to the epidemiological evidence of high HIV burden among transfeminine individuals, it also reflects a paradigm in clinical research in which trans communities are perceived as ancillary to other key communities placed at risk [13, 19]. A 2021 scoping review focusing specifically on trans populations examined 667 HIV prevention articles that sampled at least one trans participant based on assigned sex at birth found that “38.5% subsumed transgender participants into cisgender populations (most frequently combining trans women with cisgender men who have sex with men), 20.4% compared transgender and cisgender participants, and 41.1% focused exclusively on transgender women” [20••]. While this review is aimed at comprehensively providing an overview for all trans groups, data extracted were only able to delineate the inclusion of transfeminine adults in HIV studies and were unable to distinguish transmasculine and nonbinary people. To date, few reviews have been conducted to delineate the participation of either transmasculine or nonbinary individuals in HIV or PrEP studies [21], reflective of the erasure and lack of gender-inclusive approaches in PrEP studies and in the broader HIV landscape.
While there have been improvements in including transfeminine adults in PrEP and HIV research and programming, glaring intersecting gender and racial inequities remain. The inclusion of transgender and nonbinary individuals in implementation research, clinical trials, and community engagement has remained at best, scant, despite the growing number of transgender and nonbinary communities in the USA [12••]. Globally, particularly in the global south where community engagement and leadership with trans advocates have gained more prominence, PrEP programming and HIV surveillance systems are only now beginning to implement changes and correct systematic practices that subsumed trans populations into other key populations [22, 23]. And while PrEP studies and HIV surveillances have relied on sex assigned at birth as part of eligibility criteria as well as to identify trans individuals in primary data collection and in existing databases, such an approach not only disregards the diversity in trans identities but also complicates and furthers data misrepresentation rendering some to the point of invisibility, where the true burden of need remains unknown. This further limits any understanding of ethno-racial differences within subgroups of trans communities, where health inequities [24••], including HIV has been documented [25]. Trans and HIV scholars have recommended designing studies with self-reported demographic data on gender identity or trans status to be the preferred method for measuring and identifying trans populations in studies and surveillance systems, and for conducting research with trans communities [9••, 26••].
Persistence for Gender-Affirmative PrEP Systems and Trans Engagement
Advancements in PrEP have scarcely included, prioritized, or positioned trans people as stakeholders, as scientists, as partners with trans-led community-based organizations, and as we noted above, not even as research participants. This exclusion is due to the pervasiveness of cissexism and cisnormativity that leads to erasure in research and public health programming at-large that researchers—both cis and trans—reinforce and uphold [18, 27••]. Many have begun working to heal relationships between trans communities, HIV research, and scientific communities through community-engaged research and programmatic interventions [28,29,30,31,32,33,34], but much more work is needed [35]. Several trans and nonbinary scientists and community scholars working within spaces of HIV prevention have recurrently advocated for HIV prevention research and programming to be conducted with them across all stages of research development, implementation, and dissemination [17, 32].
Specifically, there has been a persistent demand by trans people for PrEP programmers to design and implement gender-affirmative PrEP systems [16]. Gender-affirmative PrEP systems necessitate for trans people to receive the necessary PrEP care continuum services [36] while also highly valuing and ensuring that trans people’s gender identity and treatment goals are medically, socially, and structurally recognized and supported—to maximize the benefits of PrEP within trans communities directly [15, 37]. In the context of HIV care, this includes the critical and comprehensive integration of HIV care with gender-affirming health services, which has been shown to improve engagement and retention for achieving viral suppression [38,39,40]. There have been some efforts to implement and evaluate gender-affirmative PrEP programs in existing healthcare settings [29, 41]; however, additional efforts are warranted to address PrEP barriers across the personal/biological, social, structural socio-ecological levels. Specifically, the transformation of health care settings towards gender-affirming warrants the implementation of policies in different geographic locales that eliminate HIV criminalization as well as bans or restrictions to legal affirmation, such as name and gender marker changes both in government-issued identification documents and electronic medical records [42]. For example, the Trans Renaming Project in Detroit, Michigan, a community-led initiative, is aimed at improving access to legal affirmation and address social and legal barriers that contribute to HIV inequities and inaccessibility to PrEP and HIV prevention services for trans communities locally [34, 43].
At the biomedical level, formative research has been conducted with transfeminine adults to examine PrEP efficacy along with gender-affirming hormones. Specifically, concerns for lowered efficacy and drug-drug interactions between PrEP and gender-affirming hormones have been documented, both from the perspectives of providers and trans community members [44, 45]. To address this concern, several pharmacological studies have examined the impact of PrEP on hormones and vice versa [45,46,47]. One pharmacological clinical trial with Thai transfeminine adults offers clarity showing that estrogen hormones do not lower PrEP efficacy in a clinically significant way and that estrogen levels were not affected by PrEP [48]. In a recent double-blind noninferiority trial with transfeminine adults, findings demonstrated that blood-level concentration of two types of PrEP formulation (emtricitabine and tenofovir alafenamide (F/TAF) versus emtricitabine and tenofovir disoproxil fumarate (F/TDF)) remained efficacious and were not negatively impacted by gender-affirming hormones [49]. However, studies on the efficacies and effectiveness of taking both gender-affirming hormones with other important PrEP modalities such as long-acting injectable PrEP and 2–1-1 are underexamined. Despite this limitation, some expert opinions convey that there are no expected drug-to-drug interactions between gender-affirming hormones and PrEP, and though more studies are needed, authors recommended to continue offering PrEP for trans communities given studies showing the reach of protective concentrations [45]. Scholars have also noted the need to train PrEP providers to utilize gender-affirming rhetoric and adopt a personalized medicine approach when prescribing gender-affirming care with PrEP [50]. This approach not only allows for providers to monitor and ensure that PrEP and hormone blood levels remain safe but also to align and meet patients’ PrEP and other HIV services needs with their gender affirmation goals [50].
At the clinic-level, a select few US- and international-based demonstration projects have shown some promising successes in implementing the integration of gender-affirming care with PrEP services, with the majority primarily designed to increase PrEP uptake among transfeminine adults in community-based health clinic settings. For example, researchers at Callen Lorde Community Health Center in New York City, an LGBTQ-focused health center that specializes in the integration of PrEP, gender-affirming care, as well as insurance and payment services, recently published a longitudinal study that showed PrEP adherence was high (greater than 90%) at 3 and 6 months after initiation both in self-report and urine assay data collection among 80% of the 100 enrolled transfeminine patients [51]. In Atlanta, a patient-centered PrEP program designed with a co-located gender clinic offering affordable comprehensive primary care, gender-affirming hormone, and mental health services showed high rates of linkage to PrEP care, prescription, and initiation among transfeminine participants. In Thailand, key population-led health service programming that offers same-day PrEP and is delivered by trained key population community health workers, including transgender lay providers, contributed to 82% current Thai PrEP users and highlighted adherence and retention as high-priority research areas for scale-up of the program [29, 52]. In addition, the Tangerine Clinic in Thailand introduced the “Integrated Trans Model,” which was disseminated to three other Asian countries using implementation strategies informed by community leaders and resulted in PrEP linkages ranged from 20 to 27% [53]. In the Philippines, community-based organizations and trans community leaders are building out grassroots community outreach, infrastructure, and organizational capacity for ongoing gender affirming care, PrEP and HIV research clinics, including offering in-person and telehealth services, training health care workforce, organizing community events, and building formal coalitions such as the Philippine Professional Association for Transgender Health to improve gender-affirming care as well as combat recent surges in HIV incidence [54]. Similarly in South Africa, scaling up of PrEP clinics are underway with aims to provide comprehensive care in addition to PrEP for transgender women, with results under review at the time of this review [55]. To our team’s knowledge, only one study in California has been inclusive of transmasculine and nonbinary communities and demonstrated high levels of PrEP initiation across gender identities; however, gender differences were found in adherence to daily oral PrEP such that transfeminine adults were more likely to have protective drug levels compared to transmasculine and nonbinary adults [41]. As such, future research is warranted to develop and implement gender-affirming PrEP programs that addresses barriers across the PrEP cascade.
Recommendations for Community-Engaged Gender-Affirming PrEP Systems
Envisioning what gender-affirming PrEP systems look like across other socio-ecological levels remains underdeveloped. Published PrEP studies typically report on outcomes rather than processes. As a step to fill this gap, we turn to documented strategies drawn from the literature, and when possible, leaned on our expertise as trans stakeholders, leaders of trans-led community organizations, and as communities of trans and cis scholars in the fields of trans health and HIV prevention to map (in Fig. 1) and synthesize the following recommendations (in Table 1).
Conclusion
Despite the development of multiple PrEP formulations now available for delivery, trans people experience suboptimal benefits due to low community engagement resulting in inequitable access and uptake of this medication. The expertise of trans people has not been adequately incorporated into the design of PrEP education and promotion campaigns. The complex health needs of trans communities have not been sufficiently consulted in the implementation of PrEP delivery systems. Consequently, trans communities continue to suffer disproportionately from the unnecessary and preventable burden of new HIV infections. This inequity must be remedied.
Meaningful and sustained investments in partnerships with trans community members are essential to mitigating widening inequities of HIV burden that disproportionately affect trans people worldwide. Specific actions are as follows: (i) recognize transmasculine and nonbinary individuals (i.e., not just transfeminine individuals) as priorities for PrEP programming; (ii) bring visibility to similarities and differences in gender-affirmation needs across the spectrum of gender minority groups by distinguishing gender-inclusive and gender-specific approaches in designing PrEP delivery systems (19); (iii) address social determinants of HIV within trans populations including—but not limited to—the role of employment, insurance, housing, legal factors that shape the ability for trans people to achieve optimal health; (iv) include trans scholars and scientists in positions of leadership in future PrEP research and programming efforts.
Notes
Transfeminine is a gender identity that describes people who were assigned male sex at birth and now with a gender identity within the transfeminine spectrum (e.g., trans women, women), and transmasculine is a gender identity that describes people who were assigned female sex at birth and now with gender identity within the transmasculine spectrum (e.g., trans men, men). And nonbinary describes people whose gender identities do not conform with the gender binary.
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Acknowledgements
We would like to thank Wesley King, PhDc, MPH, for their time and assistance in generating the graphic visualization for this manuscript.
Funding
Dr. Restar is supported by the Research Education Institute for Diverse Scholars (REIDS) Program at Yale University School of Public Health, funded by the National Institute of Mental Health (R25MH087217). Additional support was provided by R01MH115765 (Drs. Kristi Gamarel and Don Operario) from the National Institute of Mental Health (NIMH) and R21TW012010 (Dr. Don Operario) from the Fogarty International Center (FIC). This article does not represent the official views of the sponsors.
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Rena Janamnuaysook has received research funding from Gilead Sciences, and speaker fees from ViiV Healthcare. Dr. Stephaun Wallace reports research funding from NIH/NIAID, Johnson and Johnson/Janssen, and Gilead. Dr. Leigh-Ann van der Merwe reports involvement as global community advisory group for Gilead’s Lenacapavir trial for transgender women. Arjee Restar, Brian J. Minalga, Ma Irene Quilantang, Tyler Adamson, Emerson Dusic, Greg Millet, Danvic Rosadiño, Tanya Laguing, Elle Lett, Avery Everhart, Gregory Phillips II, Pich Seekaew, Kellan Baker, Florence Ashley, Jeffrey Wickersham, Don Operario, and Kristi E. Gamarel, PhD, declare that they have no conflict of interest.
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Restar, A., Minalga, B.J., Quilantang, M.I. et al. Mapping Community-Engaged Implementation Strategies with Transgender Scientists, Stakeholders, and Trans-Led Community Organizations. Curr HIV/AIDS Rep 20, 160–169 (2023). https://doi.org/10.1007/s11904-023-00656-y
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DOI: https://doi.org/10.1007/s11904-023-00656-y