ABSTRACT

Objective

The aim of this study was to investigate the prevalence of human immunodeficiency virus (HIV) infection among transgender women and travestis and to analyze factors associated with HIV infection in Brazil.

Methods

TransOdara was a cross-sectional study on sexually transmitted infections among transgender women and travestis in five Brazilian cities between 2019 and 2021. Self-identified transgender women and travestis aged ≥18 years were recruited using respondent-driven sampling, completed an interviewer-led questionnaire, and provided samples to detect HIV. The outcome was the result of the rapid antigen testing for HIV. Adjusted prevalence ratios (aPR) and 95% confidence intervals (95% CI) were obtained using Poisson regression with robust variance.

Results

Overall, this population was found to be especially vulnerable, with high levels of unstable housing and engagement in informal work. They usually resort to transactional sex as their main working activity. Half of them earned less than the Brazilian minimum wage, which characterizes a poor population living in dire conditions. The overall HIV prevalence was 34.40%. In the final model, the variables associated with the HIV prevalence were as follows: to be 31 years old or older, not studying at the moment they were interviewed, to be unemployed, and engaged in lifetime transactional sex.

Conclusion

We found disproportionately high HIV prevalence among transgender women and travestis, compared with a low prevalence among respective segments of Brazil’s general population, which highlights the context of vulnerability in this population. The data point to the urgency for intensification and expansion of access to HIV prevention and strategies to stop discrimination in health care (among other services and contexts) and provide comprehensive services for this population.

Keywords:
HIV; Travestis; Transgender persons; Prevalence; Brazil.

INTRODUCTION

The health of transgender women has been increasingly a subject of research¹1. Sweileh WM. Bibliometric analysis of peer-reviewed literature in transgender health (1900–2017). BMC Int Health Hum Rights 2018; 18(1): 16. https://doi.org/10.1186/s12914-018-0155-5
https://doi.org/10.1186/s12914-018-0155-... , given the urgent health needs of this population²2. Heng A, Heal C, Banks J, Preston R. Transgender peoples’ experiences and perspectives about general healthcare: a systematic review. Int J Transgend 2018; 19(4): 359-78. https://doi.org/10.1080/15532739.2018.1502711
https://doi.org/10.1080/15532739.2018.15...

3. Safer JD, Coleman E, Feldman J, Garofalo R, Hembree W, Radix A, et al. Barriers to healthcare for transgender individuals. Curr Opin Endocrinol Diabetes Obes 2016; 23(2): 168-71. https://doi.org/10.1097/MED.0000000000000227
https://doi.org/10.1097/MED.000000000000...

4. Winter S, Diamond M, Green J, Karasic D, Reed T, Whittle S, et al. Transgender people: health at the margins of society. Lancet 2016; 388(10042): 390-400. https://doi.org/10.1016/S0140-6736(16)00683-8
https://doi.org/10.1016/S0140-6736(16)00...

5. Reisner SL, Poteat T, Keatley JA, Cabral M, Mothopeng T, Dunham E, et al. Global health burden and needs of transgender populations: a review. Lancet 2016; 388(10042): 412-36. https://doi.org/10.1016/S0140-6736(16)00684-X
https://doi.org/10.1016/S0140-6736(16)00... -⁶6. Hughto JMW, Reisner SL, Pachankis JE. Transgender stigma and health: a critical review of stigma determinants, mechanisms, and interventions. Soc Sci Med 2015; 147: 222-31. https://doi.org/10.1016/j.socscimed.2015.11.010
https://doi.org/10.1016/j.socscimed.2015... . Global estimates of human immunodeficiency virus (HIV) prevalence among transgender women for a pool of several countries were 19.9% in the first decade of the 21st century, corresponding to an odds ratio (OR) of 66.0 when it is cross-compared with adults of reproductive age from the general population⁷7. Stutterheim SE, van Dijk M, Wang H, Jonas KJ. The worldwide burden of HIV in transgender individuals: an updated systematic review and meta-analysis. PLoS One 2021; 16(12): e0260063. https://doi.org/10.1371/journal.pone.0260063.
https://doi.org/10.1371/journal.pone.026... . The pronounced lack of any proportionality between infection rates and demographic data is made evident when cross-comparisons between transgender women and the general population are carried out, whatever the geographic unit under analysis, worldwide⁸8. Russi JC, Serra M, Viñoles J, Pérez MT, Ruchansky D, Alonso G, et al. Sexual transmission of hepatitis B virus, hepatitis C virus, and human immunodeficiency virus type 1 infections among male transvestite comercial sex workers in Montevideo, Uruguay. Am J Trop Med Hyg 2003; 68(6): 716-20. PMID: 12887033.

9. Herbst JH, Jacobs ED, Finlayson TJ, McKleroy VS, Neumann MS, Crepaz N, et al. Estimating HIV prevalence and risk behaviors of transgender persons in the United States: a systematic review. AIDS Behav 2008; 12(1): 1-17. https://doi.org/10.1007/s10461-007-9299-3
https://doi.org/10.1007/s10461-007-9299-...

10. Farías MS, Garcia MN, Reynaga E, Romero M, Vaulet MLG, Fermepín MR, et al. First report on sexually transmitted infections among trans (male to female transvestites, transsexuals, or transgender) and male sex workers in Argentina: high HIV, HPV, HBV, and syphilis prevalence. Int J Infect Dis 2011; 15(9): e635-40. https://doi.org/10.1016/j.ijid.2011.05.007
https://doi.org/10.1016/j.ijid.2011.05.0...

11. Martins TA, Kerr LRFS, Macena RHM, Mota RS, Carneiro KL, Gondim RC, et al. Travestis, an unexplored population at risk of HIV in a large metropolis of northeast Brazil: a respondent-driven sampling survey. AIDS Care 2013; 25(5): 606-12. https://doi.org/10.1080/09540121.2012.726342
https://doi.org/10.1080/09540121.2012.72... -¹²12. Costa AB, Fontanari AMV, Jacinto MM, Silva DC, Lorencetti EK, Rosa Filho HT, et al. Population-based HIV prevalence and associated factors in male-to-female transsexuals from Southern Brazil. Arch Sex Behav 2015; 44(44): 521-4. https://doi.org/10.1007/s10508-014-0386-z
https://doi.org/10.1007/s10508-014-0386-... .

Recent data highlight the unique health needs of transgender women, in addition to disproportionately higher rates of HIV infection⁷7. Stutterheim SE, van Dijk M, Wang H, Jonas KJ. The worldwide burden of HIV in transgender individuals: an updated systematic review and meta-analysis. PLoS One 2021; 16(12): e0260063. https://doi.org/10.1371/journal.pone.0260063.
https://doi.org/10.1371/journal.pone.026... ,¹³13. UNAIDS. UNAIDS Data 2022. Genova: UNAIDS; 2022. and syphilis¹⁴14. Avila MM, Farías MSR, Fazzi L, Romero M, Reynaga E, Marone R, et al. High frequency of illegal drug use influences condom use among female transgender sex workers in argentina: impact on HIV and syphilis infections. AIDS Behav 2017; 21(7): 2059-68. https://doi.org/10.1007/s10461-017-1766-x
https://doi.org/10.1007/s10461-017-1766-... . A global systematic review reported an overall prevalence of HIV infection of 19.9% among transgender women⁷7. Stutterheim SE, van Dijk M, Wang H, Jonas KJ. The worldwide burden of HIV in transgender individuals: an updated systematic review and meta-analysis. PLoS One 2021; 16(12): e0260063. https://doi.org/10.1371/journal.pone.0260063.
https://doi.org/10.1371/journal.pone.026... . The estimated prevalence for a set of Brazilian studies was even higher — 14.3% (95%CI 6.8–21.8) to 40.9% (95%CI 35.7–46.1) in 2021⁷7. Stutterheim SE, van Dijk M, Wang H, Jonas KJ. The worldwide burden of HIV in transgender individuals: an updated systematic review and meta-analysis. PLoS One 2021; 16(12): e0260063. https://doi.org/10.1371/journal.pone.0260063.
https://doi.org/10.1371/journal.pone.026... . However, there are few studies that estimate the prevalence of HIV among transgender women and travestis in Brazil. In general, the prevalence is high but varies according to the region and the methodology used by the studies. Point prevalence varied from 12 to 32% in serosurveys carried out in 2013 and 2017, respectively¹¹11. Martins TA, Kerr LRFS, Macena RHM, Mota RS, Carneiro KL, Gondim RC, et al. Travestis, an unexplored population at risk of HIV in a large metropolis of northeast Brazil: a respondent-driven sampling survey. AIDS Care 2013; 25(5): 606-12. https://doi.org/10.1080/09540121.2012.726342
https://doi.org/10.1080/09540121.2012.72... ,¹²12. Costa AB, Fontanari AMV, Jacinto MM, Silva DC, Lorencetti EK, Rosa Filho HT, et al. Population-based HIV prevalence and associated factors in male-to-female transsexuals from Southern Brazil. Arch Sex Behav 2015; 44(44): 521-4. https://doi.org/10.1007/s10508-014-0386-z
https://doi.org/10.1007/s10508-014-0386-... ,¹⁵15. Grinsztejn B, Jalil EM, Monteiro L, Velasque L, Moreira RI, Garcia ACF, et al. Unveiling of HIV dynamics among transgender women: a respondent-driven sampling study in Rio de Janeiro, Brazil. Lancet HIV 2017; 4(4): e169-e176. https://doi.org/10.1016/S2352-3018(17)30015-2
https://doi.org/10.1016/S2352-3018(17)30... ,¹⁶16. Sousa PJ, Ferreira LO, Sá JB. Descriptive study of homophobia and vulnerability to HIV/Aids of the transvestites in the Metropolitan Region of Recife, Brazil. Cien Saude Colet 2013; 18(8): 2239-51. https://doi.org/10.1590/s1413-81232013000800008
https://doi.org/10.1590/s1413-8123201300... , much higher when compared to the general Brazilian female population in 2015 (0.4%)¹⁷17. Brasil. Ministério da Saúde. Secretaria de Vigilância Sanitária. Departamento de DST, AIDS e Hepatites Virais. A resposta brasileira ao HIV e a AIDS. Relatório global de respostas a AIDS. Brasília: Ministério da Saúde; 2015..

Such inequities regarding HIV and sexually transmitted infections (STIs) can be explained by contexts of vulnerability that contribute to increased risk for HIV and other STIs: structural venerability includes poor socioeconomic conditions (e.g., when gender identity represents a barrier to ensuring stable employment and, in many contexts, housing) and difficult access to prevention and care services for HIV and other STIs (e.g., discrimination in health services by health professionals or users and a lack of qualified care)¹⁸18. Leite BO, Medeiros DS, Magno L, Bastos FI, Coutinho C, Brito AM, et al. Association between gender-based discrimination and medical visits and HIV testing in a large sample of transgender women in northeast Brazil. Int J Equity Health 2021; 20(1): 199. https//doi.org/10.1186/s12939-021-01541-z
https://doi.org/10.1186/s12939-021-01541...

19. Rocon PC, Rodrigues A, Zamboni J, Pedrini MD. Dificuldades vividas por pessoas trans no acesso ao Sistema Único de Saúde. Cien Saude Colet 2016; 21(8): 2517-26. https://doi.org/10.1590/1413-81232015218.14362015
https://doi.org/10.1590/1413-81232015218...

20. Yi S, Sok S, Chhim S, Chhoun P, Chann N, Tuot S, et al. Access to community-based HIV services among transgender women in Cambodia: findings from a national survey. Int J Equity Health 2019; 18(1): 72. https://doi.org/10.1186/s12939-019-0974-6
https://doi.org/10.1186/s12939-019-0974-... -²¹21. Sevelius JM, Patouhas E, Keatley JG, Johnson MO. Barriers and facilitators to engagement and retention in care among transgender women living with human immunodeficiency virus. Ann Behav Med 2014; 47(1): 5-16. https://doi.org/10.1007/s12160-013-9565-8
https://doi.org/10.1007/s12160-013-9565-... ; interpersonal vulnerability, such as stigma, discrimination, and violence driven by gender identity (e.g., transphobia), within social interactions creates further vulnerability to HIV²²22. Magno L, Dourado I, Silva LAV, Brignol S, Amorim L, MacCarthy S. Gender-based discrimination and unprotected receptive anal intercourse among transgender women in Brazil: a mixed methods study. PLoS One 2018; 13(4): e0194306. https://doi.org/10.1371/journal.pone.0194306
https://doi.org/10.1371/journal.pone.019...

23. Magno L, Silva LAV, Veras MA, Pereira-Santos M, Dourado I. Stigma and discrimination related to gender identity and vulnerability to hiv/aids among transgender women: a systematic review. Cad Saude Publica 2019; 35(4): e00112718. https://doi.org/10.1590/0102-311X00112718
https://doi.org/10.1590/0102-311X0011271...

24. Yi S, Ngin C, Tuot S, Chhoun P, Chhim S, Pal K, et al. HIV prevalence, risky behaviors, and discrimination experiences among transgender women in Cambodia: descriptive findings from a national integrated biological and behavioral survey. BMC Int Health Hum Rights 2017; 17(1): 14. https://doi.org/10.1186/s12914-017-0122-6
https://doi.org/10.1186/s12914-017-0122-... -²⁵25. Wilson E, Pant SB, Comfort M, Ekstrand M. Stigma and HIV risk among Metis in Nepal. Cult Health Sex 2011; 13(3): 253-66. https://doi.org/10.1080/13691058.2010.524247
https://doi.org/10.1080/13691058.2010.52... . The biological and psychosocial vulnerability dimensions are composed of sexual behaviors and practices²⁴24. Yi S, Ngin C, Tuot S, Chhoun P, Chhim S, Pal K, et al. HIV prevalence, risky behaviors, and discrimination experiences among transgender women in Cambodia: descriptive findings from a national integrated biological and behavioral survey. BMC Int Health Hum Rights 2017; 17(1): 14. https://doi.org/10.1186/s12914-017-0122-6
https://doi.org/10.1186/s12914-017-0122-... ,²⁶26. Lai J, Pan P, Lin Y, Ye L, Xie L, Xie Y, et al. A survey on HIV/AIDS-related knowledge, attitudes, risk behaviors, and characteristics of men who have sex with men among University Students in Guangxi, China. Biomed Res Int 2020; 2020: 7857231. https://doi.org/10.1155/2020/7857231
https://doi.org/10.1155/2020/7857231...

27. Van Schuylenbergh J, Motmans J, Defreyne J, Somers A, T’Sjoen G. Sexual health, transition-related risk behavior and need for health care among transgender sex workers. Int J Transgend 2019; 20(4): 388-402. https://doi.org/10.1080/15532739.2019.1617217
https://doi.org/10.1080/15532739.2019.16...

28. UNAIDS. Global HIV & AIDS statistics — fact sheet 2022. Geneva: UNAIDS; 2022.-²⁹29. Poteat T, Reisner SL, Radix A. HIV epidemics among transgender women. Curr Opin HIV AIDS 2014; 9(2): 168-73. https://doi.org/10.1097/COH.0000000000000030.
https://doi.org/10.1097/COH.000000000000... .

Condomless sex between transgender women and their sexual partners is the key proximal risk factor for HIV infection²⁹29. Poteat T, Reisner SL, Radix A. HIV epidemics among transgender women. Curr Opin HIV AIDS 2014; 9(2): 168-73. https://doi.org/10.1097/COH.0000000000000030.
https://doi.org/10.1097/COH.000000000000... . The broad picture of entangled risks comprises transactional sex⁸8. Russi JC, Serra M, Viñoles J, Pérez MT, Ruchansky D, Alonso G, et al. Sexual transmission of hepatitis B virus, hepatitis C virus, and human immunodeficiency virus type 1 infections among male transvestite comercial sex workers in Montevideo, Uruguay. Am J Trop Med Hyg 2003; 68(6): 716-20. PMID: 12887033.,⁹9. Herbst JH, Jacobs ED, Finlayson TJ, McKleroy VS, Neumann MS, Crepaz N, et al. Estimating HIV prevalence and risk behaviors of transgender persons in the United States: a systematic review. AIDS Behav 2008; 12(1): 1-17. https://doi.org/10.1007/s10461-007-9299-3
https://doi.org/10.1007/s10461-007-9299-... ,³⁰30. Nemoto T, Operario D, Keatley J, Villegas D. Social context of HIV risk behaviours among male-to-female transgenders of colour. AIDS Care 2004; 16(6): 724-35. https://doi;org/10.1080/09540120412331269567
https://doi.org/10.1080/0954012041233126...

31. Clements-Nolle K, Marx R, Guzman R, Katz M. HIV prevalence, risk behaviors, health care use, and mental health status of transgender persons: implications for public health intervention. Am J Public Health 2001; 91(6): 915-21. https://doi.org/10.2105/ajph.91.6.915
https://doi.org/10.2105/ajph.91.6.915...

32. Silva-Santisteban A, Eng S, De La Iglesia G, Falistocco C, Mazin R. HIV prevention among transgender women in Latin America: implementation, gaps and challenges. J Int AIDS Soc 2016; 19(3Suppl 2): 20799. https://doi.org/10.7448/IAS.19.3.20799
https://doi.org/10.7448/IAS.19.3.20799...

33. Poteat T, Wirtz AL, Radix A, Borquez A, Silva-Santisteban A, Deutsch MB, et al. HIV risk and preventive interventions in transgender women sex workers. Lancet 2015; 385(9964): 274-86. https://doi.org/10.1016/S0140-6736(14)60833-3
https://doi.org/10.1016/S0140-6736(14)60... -³⁴34. Guadamuz TE, Wimonsate W, Varangrat A, Phanuphak P, Jommaroeng R, McNicholl JM, et al. HIV prevalence, risk behavior, hormone use and surgical history among transgender persons in Thailand. AIDS Behav 2011; 15(3): 650-8. https://doi.org/10.1007/s10461-010-9850-5.
https://doi.org/10.1007/s10461-010-9850-... , multiple partners⁸8. Russi JC, Serra M, Viñoles J, Pérez MT, Ruchansky D, Alonso G, et al. Sexual transmission of hepatitis B virus, hepatitis C virus, and human immunodeficiency virus type 1 infections among male transvestite comercial sex workers in Montevideo, Uruguay. Am J Trop Med Hyg 2003; 68(6): 716-20. PMID: 12887033.,⁹9. Herbst JH, Jacobs ED, Finlayson TJ, McKleroy VS, Neumann MS, Crepaz N, et al. Estimating HIV prevalence and risk behaviors of transgender persons in the United States: a systematic review. AIDS Behav 2008; 12(1): 1-17. https://doi.org/10.1007/s10461-007-9299-3
https://doi.org/10.1007/s10461-007-9299-... ,³¹31. Clements-Nolle K, Marx R, Guzman R, Katz M. HIV prevalence, risk behaviors, health care use, and mental health status of transgender persons: implications for public health intervention. Am J Public Health 2001; 91(6): 915-21. https://doi.org/10.2105/ajph.91.6.915
https://doi.org/10.2105/ajph.91.6.915... ,³⁴34. Guadamuz TE, Wimonsate W, Varangrat A, Phanuphak P, Jommaroeng R, McNicholl JM, et al. HIV prevalence, risk behavior, hormone use and surgical history among transgender persons in Thailand. AIDS Behav 2011; 15(3): 650-8. https://doi.org/10.1007/s10461-010-9850-5.
https://doi.org/10.1007/s10461-010-9850-... and the misuse of substances, especially immediately before or during sex³¹31. Clements-Nolle K, Marx R, Guzman R, Katz M. HIV prevalence, risk behaviors, health care use, and mental health status of transgender persons: implications for public health intervention. Am J Public Health 2001; 91(6): 915-21. https://doi.org/10.2105/ajph.91.6.915
https://doi.org/10.2105/ajph.91.6.915... ,³²32. Silva-Santisteban A, Eng S, De La Iglesia G, Falistocco C, Mazin R. HIV prevention among transgender women in Latin America: implementation, gaps and challenges. J Int AIDS Soc 2016; 19(3Suppl 2): 20799. https://doi.org/10.7448/IAS.19.3.20799
https://doi.org/10.7448/IAS.19.3.20799... ,³⁴34. Guadamuz TE, Wimonsate W, Varangrat A, Phanuphak P, Jommaroeng R, McNicholl JM, et al. HIV prevalence, risk behavior, hormone use and surgical history among transgender persons in Thailand. AIDS Behav 2011; 15(3): 650-8. https://doi.org/10.1007/s10461-010-9850-5.
https://doi.org/10.1007/s10461-010-9850-... , altering the capacity of individuals to adopt and maintain safer sexual behaviors³⁵35. Shoptaw S, Montgomery B, Williams CT, El-Bassel N, Aramrattana A, Metsch L, et al. Not just the needle: the state of HIV prevention science among substance users and future directions. J Acquir Immune Defic Syndr 2013; 63(0 2): S174-8. https://doi.org/10.1097/QAI.0B013E3182987028
https://doi.org/10.1097/QAI.0B013E318298... , besides the obvious risks associated with the shared use of injection paraphernalia.

Epidemiological studies about HIV infection among transgender women in Brazil are relatively rare and are geographically clustered in a few places in the southeast, the southern part of the northeastern region, and, to a lesser extent, in the south⁷7. Stutterheim SE, van Dijk M, Wang H, Jonas KJ. The worldwide burden of HIV in transgender individuals: an updated systematic review and meta-analysis. PLoS One 2021; 16(12): e0260063. https://doi.org/10.1371/journal.pone.0260063.
https://doi.org/10.1371/journal.pone.026... ,³⁶36. Baral SD, Poteat T, Strömdahl S, Wirtz AL, Guadamuz TE, Beyrer C, et al. Worldwide burden of HIV in transgender women: a systematic review and meta-analysis. Lancet Infect Dis 2013; 13(3): 214-22. https://doi.org/10.1016/S1473-3099(12)70315-8
https://doi.org/10.1016/S1473-3099(12)70... . They are practically absent in the vast north and center-west regions. They do exist, but a tiny fraction of them are population-based studies of transgender women in context, besides those carried out in referral services for the prevention and treatment of this population, based on convenience samples. We aimed to investigate the regional prevalence of HIV infection among transgender women and travestis in Brazil and analyze factors associated with HIV infection.

METHODS

This is an analysis of transgender women and travestis data collected in five capital cities (Campo Grande, Manaus, Porto Alegre, Salvador, and São Paulo) located in all five Brazilian macro-regions, from December 2019 to July 2021, that composed the TransOdara study, a survey aimed at estimating the prevalence of HIV and other STIs and monitoring risk practices for these infections.

“Transgender women and travestis” is used here as an umbrella term that includes all individuals who self-identify with a gender identity different than the male sex assigned at birth.

Participants were recruited using respondent-driven sampling (RDS), a chain-link sampling method that begins with “seeds” — a convenience sample of members of the target population chosen by the researchers³⁷37. Heckathorn DD. Respondent-driven sampling: a new approach to the study of hidden populations. Soc Probl 1997; 44(2): 174-99. https://doi.org/10.2307/3096941
https://doi.org/10.2307/3096941... . In RDS, participants recruited their acquaintances using a coupon system³⁷37. Heckathorn DD. Respondent-driven sampling: a new approach to the study of hidden populations. Soc Probl 1997; 44(2): 174-99. https://doi.org/10.2307/3096941
https://doi.org/10.2307/3096941... . A maximum of three recruiters were allowed per participant to reduce recruitment homophily. The eligibility criteria were to be 18 years of age or older, to identify with a feminine gender identity at the time of study, to have been assigned male sex at birth, and to spend most of the day in the studied municipalities. They also had to present a valid invitation coupon, agree to participate in the study, and sign the informed consent form. Transgender women and travestis, who when interviewed, were under the effect or influence of drugs, including alcohol, in a manner that rendered it difficult for them to understand the research, were excluded.

The researchers selected the first participants, the so-called seeds, after qualitative formative research to represent the heterogeneity of the transgender women and travestis population according to demographic and socioeconomic conditions. In each city, 5–10 seeds launched the recruitment process. Each seed, and later each participant, received three coupons to invite transgender women and travestis from their social contact network (referral chains). For successful recruitment, RDS includes primary and secondary incentives. The primary one was US$10.00 as compensation for transportation and lost work time. The secondary one, as compensation for the recruitment of contacts, was US$10.00 for each transgender women and travestis recruited for the study. All completed a standard investigator-led questionnaire for sociodemographic information and sexual behavior, in a space reserved exclusively for this purpose. Further details are found in Veras et al.³⁸38. Veras MASM, Pinheiro TF, Galan L, et al. TransOdara study: the challenge of integrating methods, settings and procedures during the COVID-19 pandemic in Brazil. Rev Bras Epidemiol. 2024; 27(Suppl 1): e240002.supl.1. https://doi.org/10.1590/1980-549720240002.supl.1
https://doi.org/10.1590/1980-54972024000...

Study variables

The outcome variable was the result of the rapid antigen HIV test, classified as positive or negative. Other study variables used in this study were gender identity (transgender women and travestis versus travesti versus agender/other female identification), sexual orientation (heterosexual versus bisexual/pansexual/homosexual/gay/lesbian/asexual/other) age (18–30 years versus 31–68 years), self-reported race/skin color (whites versus blacks/brown), studying at the moment they were interviewed (yes versus no); schooling (no education/only primary-level versus secondary-level education versus higher education); living situation (stable: own house or apartment, rented house or apartment versus unstable: family and friends, street situation; shelter or boarding house); occupation (employee with a formal contract versus employee without a formal contract versus unemployed); minimum wage in Brazilian reais (one or less versus more than one); and lifetime transactional sex work (no versus yes).

Data analysis

The sociodemographics of the study population were described according to the results of the HIV test. The associations between the study variables and HIV prevalence were measured by the prevalence ratio (PR) with the respective 95% CI in bivariate and multivariate analyses using a mixed Poisson regression with robust variance (a useful tutorial for beginners using R is available at https://stats.oarc.ucla.edu/r/dae/poisson-regression/).

Random intercepts have been applied to each one of the sites (i.e. the respective cities) included in the multicenter study. The choice of using random intercepts is secondary to the between-site heterogeneity, both respecting HIV background infection rates and the sociodemographic characteristics of each site.

Using the abovementioned model, we assumed that we could capture (at least partially) the effects secondary to the different heterogeneities. We took into consideration the American Statistical Association (ASA) statement³⁹39. Wasserstein RL, Lazar NA. The ASA’s statement on p-values: context, process, and purpose. Am Stat 2016; 70(2): 129-33. https://doi.org/10.1080/00031305.2016.1154108
https://doi.org/10.1080/00031305.2016.11... , i.e. considering that every statistical test should be understood in the context of its application, analytic procedures, and purpose. Weighting was not included in the analyses as suggested by Sperandei et al.⁴⁰40. Sperandei S, Bastos LS, Ribeiro-Alves M, Reis A, Bastos FI. Assessing logistic regression applied to respondent-driven sampling studies: a simulation study with an application to empirical data. Int J Soc Res Methodol 2023; 26(3): 319-33. https://doi.org/10.1080/13645579.2022.2031153
https://doi.org/10.1080/13645579.2022.20... , respecting the differential accuracy of RDS indicators for underlying networks with varying natures.

The variables with a p-value≤0.20 in the bivariate analysis were selected to start modeling, and those with a p-value<0.05 remained in the final model, along with variables that were theoretically important, using the backward approach. The adequacy of the final models was analyzed using the Akaike information criteria. All analyses were conducted using R version 4.2.0⁴¹41. R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2022., comprising libraries lme4 and statistical models.

Ethical aspects

The project was approved by the Research Ethics Committee of the Santa Casa de Misericórdia de São Paulo (CAAE 05585518.7.0000.5479; opinion n°: 3.126.815 – 30/01/2019), as well as by other participating institutions: Instituto Leônidas and Maria Deane-ILMD/Fiocruz – Manaus; STD/AIDS Reference and Training Center, Instituto Adolfo Lutz; Municipal Secretary of Health of Porto Alegre; Federal University of Bahia; Federal University of Mato Grosso do Sul-UFMS, Federal University of Health Sciences of Porto Alegre; and Federal University of Rio Grande do Sul-UFRS. Written informed consent was obtained from all individual participants included in the study. Transgender women and travestis were involved in the design and implementation of the study and led the recruitment of participants using RDS.

RESULTS

Of the 1,317 transgender women and travestis recruited and interviewed, 1,282 (97.3%) agreed to be tested for HIV. Among them, the overall prevalence was 34.40% (95%CI 31.8–37.1%) (number of positives=441). According to each city, the estimated prevalence was 26.55% (107) for São Paulo, 27.59% (48) for Campo Grande, 31.46% (56) for Salvador, 36.69% (124) for Manaus, and 56.08% (106) for Porto Alegre.

Most interviewees self-defined themselves as women or transsexual women (66.6%), heterosexual (79.2%), or aged up to 30 years (50.9%). A substantial majority self-defined themselves as Black (45.6%) and were not studying at the moment they were interviewed (78.6%). Slightly above half of them (52.1%) had completed high school, lived in unstable housing conditions (74.2%), have been engaged in informal work (79.7%), and had lifetime transactional sex as their main working activity (73.7%). Half (50.9%) earned less than the Brazilian minimum wage per month (Table 1).

In the bivariate analyses, the key variables associated with HIV prevalence were found to identify as a travesti (PR: 2.27; 95%CI 1.11–4.63), to report heterosexual as sexual orientation (PR: 1.43; 95%CI 1.10–1.85), not studying at the moment they were interviewed (PR: 1.49; 95%CI 1.15–1.93), to be engaged in informal work (PR: 1.51; 95%CI 1.02–2.22) or unemployed (PR: 1.80; 95%CI 1.14–2.86), as well as to be engaged in lifetime transactional sex (PR: 1.97; 95%CI 1.52–2.55) (Table 1).

In the final multivariate model, the variables independently associated with the outcome (HIV prevalence) were the ones as follows: to be 31 years old or more (PR: 1.76; 95%CI 1.44–2.16), not studying at the moment they were interviewed (1.32; 95%CI 1.01–1.73), to be unemployed (1.76; 95%CI 1.10–2.80), and to be engaged in lifetime transactional sex (1.76; 95%CI 1.35–2.29) (Table 2).

DISCUSSION

This study has made evident a very high pooled prevalence for HIV among the large number of transgender women and travestis interviewed, as well as a high point prevalence for each one of the sites included in the multicenter study, ranging from 26.32 to 56.08%.

The results corroborate previous findings from both population-based studies as well as studies with convenience samples from referral centers⁷7. Stutterheim SE, van Dijk M, Wang H, Jonas KJ. The worldwide burden of HIV in transgender individuals: an updated systematic review and meta-analysis. PLoS One 2021; 16(12): e0260063. https://doi.org/10.1371/journal.pone.0260063.
https://doi.org/10.1371/journal.pone.026... . Whatever the setting and the sampling strategy, HIV infection rates are always very high and much higher than those observed among women in the general population⁷7. Stutterheim SE, van Dijk M, Wang H, Jonas KJ. The worldwide burden of HIV in transgender individuals: an updated systematic review and meta-analysis. PLoS One 2021; 16(12): e0260063. https://doi.org/10.1371/journal.pone.0260063.
https://doi.org/10.1371/journal.pone.026... .

One of the hypotheses for the much higher rate in Porto Alegre is the specificity of the epidemic in Rio Grande do Sul (RS). The acquired immune deficiency syndrome (AIDS) detection rate in RS (24.3 per 100,000 inhabitants) in 2022 was one and a half times higher than that for the country (16.5 per 100,000 inhabitants). The mortality rate was also higher (7.7 deaths per 100,000 inhabitants) in RS than the national average, which was 4.2 deaths per 100,000 inhabitants. The highest mortality rate was estimated for Porto Alegre (22.6 deaths per 100,000 inhabitants), five times the national rate. According to the composite index based on the indicators of AIDS detection rate, mortality rate, and first CD4 cell count in the past five years, Porto Alegre ranked in the second highest position among the Brazilian capitals⁴²42. Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Doenças de Condições Crônicas e Infecções Sexualmente Transmissíveis. Boletim Epidemiológico de HIV/Aids. Brasília: Ministério da Saúde; 2022..

In a population deeply affected by stigma and marginalization⁶6. Hughto JMW, Reisner SL, Pachankis JE. Transgender stigma and health: a critical review of stigma determinants, mechanisms, and interventions. Soc Sci Med 2015; 147: 222-31. https://doi.org/10.1016/j.socscimed.2015.11.010
https://doi.org/10.1016/j.socscimed.2015... ,²³23. Magno L, Silva LAV, Veras MA, Pereira-Santos M, Dourado I. Stigma and discrimination related to gender identity and vulnerability to hiv/aids among transgender women: a systematic review. Cad Saude Publica 2019; 35(4): e00112718. https://doi.org/10.1590/0102-311X00112718
https://doi.org/10.1590/0102-311X0011271... ,⁴³43. Magno L, Dourado I, Silva LAV. Estigma e resistência entre travestis e mulheres transexuais em Salvador, Bahia, Brasil. Cad Saude Publica 2018; 34(5): e00135917. https://doi.org/10.1590/0102-311x00135917
https://doi.org/10.1590/0102-311x0013591... , living in dire conditions characterized by unstable housing⁴³43. Magno L, Dourado I, Silva LAV. Estigma e resistência entre travestis e mulheres transexuais em Salvador, Bahia, Brasil. Cad Saude Publica 2018; 34(5): e00135917. https://doi.org/10.1590/0102-311x00135917
https://doi.org/10.1590/0102-311x0013591...

44. Vartabedian J. Migraciones trans: Travestis Brasileñas migrantes trabajadoras del sexo en Europa. Cad Pagu 2014; (42): 275-312.; https://doi.org/10.1590/0104-8333201400420275
https://doi.org/10.1590/0104-83332014004... -⁴⁵45. Padilla MB, Rodríguez-Madera S, Varas-Díaz N, Ramos-Pibernus A. Trans-migrations: border-crossing and the politics of body modification among Puerto Rican transgender women. Int J Sex Health 2016; 28(4): 261-77. https://doi.org/10.1080/19317611.2016.1223256
https://doi.org/10.1080/19317611.2016.12... , enormous difficulties engaging in the formal labor market, low income, and frequent unemployment⁴⁶46. Silva MA, Luppi CG, Veras MASM. Work and health issues of the transgender population: factors associated with entering the labor market in the state of São Paulo, Brazil. Cien Saude Colet 2020; 25(5): 1723-34. https://doi.org/10.1590/1413-81232020255.33082019
https://doi.org/10.1590/1413-81232020255...

47. Bonassi BC, Amaral MS, Toneli MJF, Queiroz MA. Vulnerabilidades mapeadas, Violências localizadas: Experiências de pessoas travestis e transexuais no Brasil. Quad Psicol (Bellaterra, Internet) 2015; 17(3): 83-98. https://doi.org/10.5565/rev/qpsicologia.1283
https://doi.org/10.5565/rev/qpsicologia.... -⁴⁸48. Nadal KL, Davidoff KC, Fujii-Doe W. Transgender women and the sex work industry: roots in systemic, institutional, and interpersonal discrimination. J Trauma Dissociation 2014; 15(2): 169-83. https://doi.org/101080/152997322014867572
https://doi.org/101080/15299732201486757... , this inauspicious finding is by no means surprising. The several adverse conditions and risk factors tend to cluster and frequently interact, all of them contributing to unacceptable living standards and high vulnerability to HIV (among other infections and other medical and social conditions not assessed in the current study).

In Brazil, HIV prevalence in this population is very high and seems unlikely to be curbed or even substantially ameliorated, with the exception of women who benefit from state-of-the-art prevention programs, including pre-exposure prophylaxis (PrEP)⁴⁹49. Magno L, Medeiros DS, Soares F, Grangeiro A, Caires P, Fonseca T, et al. Factors associated to HIV prevalence among adolescent men who have sex with men in Salvador, Bahia State, Brazil: baseline data from the PrEP1519 cohort. Cad Saude Publica 2023; 39 (Suppl 1): e00154021. https://doi.org/10.1590/0102-311XEN154021
https://doi.org/10.1590/0102-311XEN15402...

50. Veloso VG, Cáceres CF, Hoagland B, Moreira RI, Vega-Ramírez H, Konda KA, et al. Same-day initiation of oral pre-exposure prophylaxis among gay, bisexual, and other cisgender men who have sex with men and transgender women in Brazil, Mexico, and Peru (ImPrEP): a prospective, single-arm, open-label, multicentre implementation study. Lancet HIV 2023; 10(2): e84-e96. https://doi.org/10.1016/S2352-3018(22)00331-9
https://doi.org/10.1016/S2352-3018(22)00...

51. Dourado I, Soares F, Magno L, Amorim L, Filho ME, Leite B, et al. Adherence, safety, and feasibility of HIV Pre-Exposure Prophylaxis among adolescent men who have sex with men and transgender women in Brazil (PrEP1519 study). J Adolesc Health 2023; 73(6S): S33-S42. https://doi.org/10.1016/j.jadohealth.2023.09.005
https://doi.org/10.1016/j.jadohealth.202... -⁵²52. Dourado I, Magno L, Greco DB, Zucchi EM, Ferraz D, Westin MR, et al. Interdisciplinarity in HIV prevention research: the experience of the PrEP1519 study protocol among adolescent MSM and TGW in Brazil. Cad Saude Publica 2023; 39(Suppl 1): e00143221. https://doi.org/10.1590/0102-311XEN143221
https://doi.org/10.1590/0102-311XEN14322... .

A systematic review and meta-analysis of Brazilian studies implemented between 1995 and 2016 made evident prevalence rates varying between 14.3% (6.8–21.8) and 40.9 (35.7–46.1)⁷7. Stutterheim SE, van Dijk M, Wang H, Jonas KJ. The worldwide burden of HIV in transgender individuals: an updated systematic review and meta-analysis. PLoS One 2021; 16(12): e0260063. https://doi.org/10.1371/journal.pone.0260063.
https://doi.org/10.1371/journal.pone.026... . More recent studies have shown point prevalence’s slightly lower, despite the fact that confidence intervals still tend to overlap, varying from 9.0% (4.2–18.2) to 31.2% (18.8–43.6) for studies carried out in Salvador⁵³53. Leite BO, Magno L, Soares F, MacCarthy S, Brignol S, Bastos FI, et al. HIV prevalence among transgender women in Northeast Brazil – findings from two respondent driven sampling studies. BMC Public Health 2022; 22(1): 2120. https://doi.org/10.1186/s12889-022-14589-5
https://doi.org/10.1186/s12889-022-14589... and Rio de Janeiro¹⁵15. Grinsztejn B, Jalil EM, Monteiro L, Velasque L, Moreira RI, Garcia ACF, et al. Unveiling of HIV dynamics among transgender women: a respondent-driven sampling study in Rio de Janeiro, Brazil. Lancet HIV 2017; 4(4): e169-e176. https://doi.org/10.1016/S2352-3018(17)30015-2
https://doi.org/10.1016/S2352-3018(17)30... , respectively.

Since sampling errors tend to be ignored (in the case of convenience samples) or are very hard to estimate (in the case of studies using the available alternatives to probability studies, such as RDS), it is difficult to distinguish trends toward a putative decline of infection rates in recent years from biases secondary to statistical inference in non-probability samples⁵⁴54. Elliott MR, Valliant R. Inference for nonprobability samples. Statist Sci 2017; 32(2): 249-64. https://doi.org/101214/16-STS598
https://doi.org/101214/16-STS598... .

High prevalence rates have also been shown in studies in Argentina (34.1%)⁵⁵55. Farías MSR, Garcia MN, Reynaga E, Romero M, Vaulet MLG, Fermepín MR, et al. First report on sexually transmitted infections among trans (male to female transvestites, transsexuals, or transgender) and male sex workers in Argentina: high HIV, HPV, HBV, and syphilis prevalence. Int J Infect Dis 2011; 15(9): e635-40. https://doi.org/10.1016/j.ijid.2011.05.007
https://doi.org/10.1016/j.ijid.2011.05.0... and Uruguay (21.5%)⁸8. Russi JC, Serra M, Viñoles J, Pérez MT, Ruchansky D, Alonso G, et al. Sexual transmission of hepatitis B virus, hepatitis C virus, and human immunodeficiency virus type 1 infections among male transvestite comercial sex workers in Montevideo, Uruguay. Am J Trop Med Hyg 2003; 68(6): 716-20. PMID: 12887033.. Of much concern is the fact that prevalence rates are almost invariably higher than the single pooled estimate for this population worldwide (point prevalence of 19.9%)⁷7. Stutterheim SE, van Dijk M, Wang H, Jonas KJ. The worldwide burden of HIV in transgender individuals: an updated systematic review and meta-analysis. PLoS One 2021; 16(12): e0260063. https://doi.org/10.1371/journal.pone.0260063.
https://doi.org/10.1371/journal.pone.026... .

In Brazil and in the vast majority of countries and specific settings, transgender women live in contexts of high vulnerability and face stigmatization and marginalization on a daily basis⁵5. Reisner SL, Poteat T, Keatley JA, Cabral M, Mothopeng T, Dunham E, et al. Global health burden and needs of transgender populations: a review. Lancet 2016; 388(10042): 412-36. https://doi.org/10.1016/S0140-6736(16)00684-X
https://doi.org/10.1016/S0140-6736(16)00... ,²³23. Magno L, Silva LAV, Veras MA, Pereira-Santos M, Dourado I. Stigma and discrimination related to gender identity and vulnerability to hiv/aids among transgender women: a systematic review. Cad Saude Publica 2019; 35(4): e00112718. https://doi.org/10.1590/0102-311X00112718
https://doi.org/10.1590/0102-311X0011271... ,⁵⁶56. Jesus JG, Belden CM, Huynh HV, Malta M, LeGrand S, Kaza VGK, et al. Mental health and challenges of transgender women: a qualitative study in Brazil and India. Int J Transgend Health 2020; 21(4): 418-30. https://doi.org/10.1080/26895269.2020.1761923
https://doi.org/10.1080/26895269.2020.17...

57. Fredriksen-Goldsen KI, Cook-Daniels L, Kim HJ, Erosheva EA, Emlet CA, Hoy-Ellis CP, et al. Physical and mental health of transgender older adults: an at-risk and underserved population. Gerontologist 2014; 54(3): 488-500. https://doi.org/10.1093/geront/gnt021
https://doi.org/10.1093/geront/gnt021... -⁵⁸58. Valentine SE, Shipherd JC. A systematic review of social stress and mental health among transgender and gender non-conforming people in the United States. Clin Psychol Rev 2018; 66: 24-38. https://doi.org/10.1016/j.cpr.2018.03.003
https://doi.org/10.1016/j.cpr.2018.03.00... . Brazil remains the country where violence against transgender women is more prevalent, with a very high level of homicides (vis-à-vis the relatively small denominators)⁵⁹59. Transgender Europe. Guidelines to human rights-based trans-specific healthcare. transgender Europe [Internet]. 2019 [cited on June 12, 2023]. Available from: https://tgeu.org/guidelines-to-human-rights-based-trans-specific-healthcare/
https://tgeu.org/guidelines-to-human-rig... ,⁶⁰60. Benevides BG. Dossiê: assassinatos e violências contra travestis e transexuais brasileiras em 2022. Brasília: Associação Nacional de Travestis e Transexuais; 2023.. Despite the undeniable gains of targeted projects, this unfortunate situation calls for structural changes, with the deep commitment of the government at different levels and civil society.

A comprehensive set of coordinated initiatives is sorely needed, combining targeted interventions (e.g., in the field of health) with structural changes, increasing the chances that this population may have full access to education, employment, and working opportunities in different types of jobs, especially those currently far from accessible, i.e., well-paid, high-qualified jobs⁶¹61. European Commission. On the implementation of the LGBTIQ equality strategy 2020-2025. Luxembourg: Publications Office of the European Union; 2023. https://doi.org/10.2838/909738
https://doi.org/10.2838/909738...

62. Brasil. Ministério da Saúde. Gabinete do Ministro. Comissão Intergestores Tripartite. Resolução no 26, de 28 de setembro de 2017. Dispõe sobre o II Plano Operativo (2017-2019) da Política Nacional de Saúde Integral de Lésbicas, Gays, Bissexuais, Travestis e Transexuais (Política Nacional de Saúde Integral LGBT) no âmbito do Sistema Único de Saúde [Internet]. Diário Oficial da União de 28 de setembro de 2017 [cited on June 16, 2023]. Available from: https://bvsms.saude.gov.br/bvs/saudelegis/cit/2017/res0026_27_10_2017.html
https://bvsms.saude.gov.br/bvs/saudelegi...

63. Mello L, Perilo M, Braz CA, Pedrosa C. Políticas de saúde para lésbicas, gays, bissexuais, travestis e transexuais no Brasil: em busca de universalidade, integralidade e equidade. Sex Salud Soc (Rio J) 2011; 9: 7-28. https://doi.org/10.1590/s1984-64872011000400002
https://doi.org/10.1590/s1984-6487201100...

64. Brasil. Ministério da Saúde. Secretaria de Gestão Estratégica e Participativa. Departamento de Apoio à Gestão Participativa. Política nacional de saúde integral de lésbicas, gays, bissexuais, travestis e transsexuais. Brasília: Ministério da Saúde; 2013.-⁶⁵65. Popadiuk GS, Oliveira DC, Signorelli MC. A política nacional de saúde integral de lésbicas, gays, bissexuais e transgêneros (LGBT) e o acesso ao processo transexualizador no sistema Único de Saúde (SUS): avanços e desafios. Ciênc Saúde Colet 2017; 22(5): 1509-20. https://doi.org/10.1590/1413-81232017225.32782016
https://doi.org/10.1590/1413-81232017225... . The high rates of engagement in the informal market, the high rates of unemployment, and the very low income of the vast majority of these women show such goals remain a dream rather than concrete opportunities.

A deep gap remains between what has been promised and has been several times translated into non-discriminatory laws and initiatives. Of course, such legal benchmarks are essential, but they should be translated into practical and continuous initiatives. Prejudice is deeply entrenched and pervasive. The fight to curb it must be as present and relentless as its open and disguised roots.

It is not clear whether HIV infection rates are really decreasing in recent years or that the putative trends may be just a consequence of many gaps, caveats, and biases. Whatever the truth, the real or perceived decrease is too slow and will cost the lives of several people. People have already been victimized by homicides and other severe medical conditions. These figures are not compatible with what we could call a humane and compassionate society.

This study has limitations. The cross-sectional design poses challenges in capturing temporal relationships within the explored associations. The RDS methodology’s design may introduce selection bias through non-probabilistic sampling and network homophily, though it does not rule out the feasibility of conducting such inquiries in hard-to-reach populations. To minimize drawing bias, statistical analyses incorporated the city as a random intercept in the mixed-effects Poisson regression models. Nevertheless, these limitations do not preclude us from gathering valuable information about the contact networks of our sample, aligning with other findings in the literature.

Despite Brazil making progress with public policies (e.g., the National Policy on STIs/AIDS and the National Policy on LGBT Integral Health), many barriers remain, consequently impeding the full implementation of HIV prevention strategies. Gender discrimination has been described in the literature as a structuring factor of social inequities for the transgender population, particularly in increasing the vulnerability of transgender women and travestis to HIV infection. This study reinforces the need to prioritize the right to dignified social well-being and quality of life, as well as clearly indicating the urgency to intensify and expand access to HIV prevention and the implementation of strategies that disrupt the discrimination experienced in healthcare services (among others) and provide appropriate services for this population.

ACKNOWLEDGMENTS:

We would like to express our gratitude to the transgender women and travestis who participated in the TransOdara study across five capital cities in Brazil. We also thank the staff of the Brazilian Ministry of Health, Department of Chronic Conditions and Sexually Transmitted Infections (DCCI), particularly Cristina Pimenta and Silvana Giozza, and of the Pan American Health Organization (PAHO), especially Grasiela Araújo.

REFERENCES

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