High HIV prevalence among transgender women in Paraguay

Abstract

Transgender women have been understudied and underserved in Paraguay; data are urgently needed to understand their HIV prevention and care needs. To estimate HIV prevalence and related risk and preventive behaviors among trans women in Paraguay, we conducted a cross-sectional survey in 2017. We employed starfish sampling – a hybrid venue-based and peer-referral method combining recruitment at randomly sampled venues and randomly selected clients from program lists, followed by short-chain referrals of eligible peers. Among 304 trans women enrolled, HIV prevalence was 24.8% (95% confidence interval [CI] 18.5–31.2%), with risk increasing with age (adjusted odds ratio [AOR] 1.06 per year, 95% CI 1.03–1.10), residence in Asunción department (AOR 4.75, 95% CI 1.57–14.36), and cocaine use (AOR 2.09, 95% CI 1.11–3.95). Trans women in Paraguay need to be prioritized for interventions with high HIV prevention efficacy. Substance use interventions to address cocaine use may also yield prevention benefits for trans women in our context.

Keywords

South America HIV high-risk behavior sexual behavior women

Introduction

Evidence worldwide indicates that transgender women (hereafter ‘trans women’) have the highest burden of HIV, with 49 times the odds of being HIV-infected compared to the general populace.¹ Where data are available, Latin America’s HIV epidemic is similarly disproportionately concentrated in trans women.¹,² For example, research from Peru and Brazil find HIV prevalence at 30% among trans women in both countries.³,⁴

Most studies point to sexual risk behavior as the primary mode of HIV transmission for trans women.^5–8 Other studies document the relationship between sex work and HIV risk among trans women who may be vulnerable to engaging in unsafe sex due to violence and high pay offered for not using condoms.⁹,¹⁰ Trans women with cisgender male partners face a high HIV transmission probability via condomless anal sex with serodiscordant and viremic partners.¹¹ Social marginalization also contributes to the high burden of HIV by limiting the provision and uptake of services for trans women, and by forcing them into risky environments including sex work for economic survival.¹²,¹³ Substance use may also be a driver of sexual risk and subsequent HIV infection among trans women. One study in neighboring Brazil found cocaine use among trans women common and significantly associated with HIV infection.³ One previous study conducted in Paraguay among female sex workers (FSWs) and men who have sex with men (MSM) found cocaine use had an adjusted odds ratio of 6.61 for HIV infection among MSM.¹⁴ However, cocaine use and its potential association with HIV among trans women has not been measured in Paraguay.

In order to end the HIV epidemic in Latin America, Paraguay and other countries in the region need to better understand the conditions that lead to the high levels of infection among trans women and develop culturally-tailored, evidence-based approaches to prevention and care. At present, there are few studies on HIV prevalence among trans women in Latin America and, to our knowledge, none from Paraguay, to advocate for and guide prevention and care interventions. This study was therefore conducted to fill these critical epidemiologic data gaps.

Materials and methods

Study population and sampling methods

The study aimed to estimate HIV prevalence and related risk and preventive factors in the population of trans women in Paraguay in 2017. Eligible participants were 15 years old and above who lived or worked in five major departments of Paraguay, including Asunción, Central, Caaguazú, Guairá, and Alto Paraná. These five departments were selected from a total of 17 in the country, because they were accessible and include the majority of the population of Paraguay, many of its major urban areas, and the capital. For inclusion in the survey, trans women were defined as persons self-reporting as being assigned male sex at birth who currently identified on the feminine gender spectrum, regardless of use of gender transition methods or presentation.

Trans women are a hidden population in Paraguay due to stigma and discrimination that creates vulnerability for violence. To efficiently reach trans women for this study, we used a hybrid sampling design called ‘starfish sampling’ that was previously developed for research with trans men in San Francisco, USA.¹⁵ Starfish sampling combines venue-based and peer-referral methods. Sampling entails creating a map or ‘universe’ of venues where trans women can be found and randomizing these sources for recruitment, as in time-location sampling.¹⁵,¹⁶ Venue-based recruitment is followed by enlisting participants to refer eligible peers from their social networks, as in respondent-driven sampling,¹⁶ although typically resulting in shorter chains of recruitment.¹⁵ The mapping of venues included sites where trans women are engaged in sex work and places where our partnering non-governmental organizations (NGOs) provide outreach. The present study added the random selection of clients of programs serving trans women for recruitment and for peer referrals. Starfish sampling adds a probability basis by starting with recruitment of trans women at randomly selected venues and among clients. The peer referral component diversifies the sample away from these sources to include trans women who are not present in the mapped sites, are not accessing programs, and may not do sex work.

The study began with a formative investigation that included ﬁeld observation and key informant interviews with trans women (N = 12). Key informants were trans women referred to the study by two partnering national NGOs. Their participation, following verbal consent, was anonymous. Open-ended questions guided discussion on the places where trans women congregate, their numbers in different venues and neighborhoods, including for sex work, hours when they could be found, and willingness to refer other trans women to the study. Key informants expanded the map beyond the outreach sites known to the NGOs. The formative phase also used observation to map trans women sex worker sites and neighborhoods where trans women resided. The mapping was done using trans women peers, outreach workers and key informants, as guides. From the NGO outreach program, key informant interviews, and field observation, a recruitment roster was developed. The ﬁrst phase of recruitment consisted of randomly sampling from the roster of the mapped sites and the client list. All trans women encountered at the mapped sites and those selected from the client list were invited to participate. In the second phase, we asked participants recruited from the mapped sites and client list to refer other trans women they knew. The number to be referred was not limited. Referred trans women participants who agreed to participate were scheduled a study visit by the research team. Due to anticipated low literacy, participants received an interviewer-administered survey. Upon completion of the interview, pre-test counseling and rapid HIV testing were provided following standard protocols. Participants in the formative and survey phases were given food, refreshment, and per diem plus travel allowance.

Measures

Demographic characteristics included age, department of residence, education, and employment. Sexual behavior indicators included age at first sex, sexual partner types, and if they used a condom the last time they had sex with each type of partner. Those with exchange partners were asked if they used alcohol before sex with their last exchange partner. Exchange partners were defined as those who gave money or goods or provided for other needs (e.g. rent, clothes, food). Participants were asked if they ever used cocaine or crack and how often. Participants who reported using cocaine or crack one or more times per week for at least 25 days in the last six months were categorized as having high-risk cocaine use. Participants were asked if they had a sexual partner in the last six months whose HIV status they did not know and if they had condomless sex with the partner of unknown status. HIV testing ever and in the last six months were assessed. Participants were also asked if they knew where to get a free condom, whether they were ever approached by a HIV prevention worker, and whether they received a condom from a HIV prevention program in the last 12 months.

To determine HIV prevalence, participants were offered onsite rapid testing, following national protocols, using HIV-1/2 STAT Pak Assay (Chembio Diagnostic Systems, NY, USA) and SD BIOLINE HIV-1/2 3.0 (Standard Diagnostics, Inc., Korea). For confirmation, a venous blood sample was obtained from all participants whose rapid test was positive and from one in ten participants whose test was negative for quality assurance purposes by a trained laboratory technician. Post-test counseling was provided; newly diagnosed persons were linked to the HIV reference centers in each department. We assessed if participants testing HIV-positive were previously diagnosed by matching an alphanumeric code generated by groups of letters in their name following the same algorithm used for the national HIV clinical care database (i.e. that they had been previously linked to care).

Statistical analysis

Statistical analysis adjusted standard errors for the starfish sampling design using the random primary sampling unit of the venue or initial contacted client with their affiliated referrals as part of the cluster. Point estimates are shown with adjusted 95% confidence intervals (CIs). Bivariate logistic regression analysis estimated odds ratios (ORs) for associations between HIV infection and independent demographic and behavioral variables. Multivariate logistic regression was used to determine independent factors associated with HIV. Covariates were entered in the model if they had p < 0.10 in bivariate analysis and reported as significant at p < 0.05. Statistical analysis was conducted using Stata 14® (StataCorp. 2015. Stata Statistical Software: Release 14. College Station, TX: StataCorp LP).

Ethical considerations

The study protocol was reviewed and approved by the Internal Review Board of the Tropical Medicine Institute of the Ministry of Health of Paraguay. Written informed consent was obtained from all participants. In accordance with laws in Paraguay, if the participant was a minor, the consent of the responsible adult was required in addition to their assent.

Results

A total of 304 trans women were recruited in 61 clusters as primary sampling units (average five per cluster, range 1–26, including 23 with only one recruit in each). The sample was notably young, with 34.8% between ages 15 and 24 years old (Table 1). The largest numbers resided in the Central (45.7%) and Asunción (37.2%) departments. More than half (56.6%) had less than a secondary education. Only 2.0% had completed university. Almost all (95.7%) had been employed in work other than sex work in the last year.

Table 1.

Demographic characteristics of transgender women, Paraguay, 2017 (N = 304).

Characteristic	n (%)	95% Confidence interval^a
Age group in years
15–19	22 (7.2)	4.3–10.2
20–24	84 (27.6)	22.6–32.6
25–29	64 (21.1)	15.8–26.3
30–34	53 (17.4)	11.9–22.9
35–39	38 (12.5)	8.6–16.4
Above 39	43 (14.1)	10.1–18.2
Department of current residence
Central	139 (45.7)	31.9–59.6
Asunción	113 (37.2)	23.8–50.5
Alto Paraná	30 (9.9)	3.3–23.0
Caaguazú	13 (4.3)	1.9–10.5
Guairá	9 (3.0)	2.9–8.9
Highest education level completed
Primary, incomplete	19 (6.4)	2.3–10.6
Primary, complete	35 (11.9)	8.3–15.5
Secondary, incomplete	113 (38.3)	33.3–43.3
Secondary, complete	107 (36.3)	30.0–42.5
Vocational training, incomplete	7 (2.4)	0.6–4.2
Vocational training, complete	2 (0.7)	0.3–1.6
University, incomplete	6 (2.0)	0.3–3.7
University, complete	6 (2.0)	0.1–4.2
Employed in last 12 months (other than sex work)
No	16 (5.3)	1.9–8.6
Yes	288 (95.7)	91.4–98.1

^aAdjusted for sampling design.

Of the 304 trans women interviewed and tested, 75 were confirmed HIV-positive by Western Blot (Table 2). One trans women was positive on rapid testing but negative on Western Blot and was classified as negative in the present analysis. Two other trans women testing positive on rapid test declined to provide a specimen for confirmatory testing. Moreover, they were not found in the HIV care clinic database. They were also removed from the analysis of HIV prevalence. The overall HIV prevalence excluding these cases was 24.8% (75 of 302, 95% CI 18.5–31.2). Among those confirmed as HIV-positive, 61 (81.3%, 95% CI 73.5–89.2) were matched to patients in the clinical care database and therefore previously diagnosed. The remaining 14 reported that they had not previously tested positive and were not matched to patients in the clinic database (i.e. they were new diagnoses).

Table 2.

HIV prevalence and sexual- and drug use-related behaviors, transgender women, Paraguay, 2017 (N = 304).

Variable (number of respondents or sub-group)	N (%)	95% Confidence interval^a
HIV-positive (n = 302)	75 (24.8)	18.5–31.2
Previously diagnosed with HIV (n = 75)	61 (81.3)	73.5–89.2
Age at first oral, anal, or vaginal sex <15 years (n = 304)	179 (58.9)	51.5–66.3
Stable partner, last six months (n = 304)	107 (35.2)	29.6–40.8
Condom use at last sex (n = 107)	42 (39.3)	28.2–50.3
Casual partner, last six months (n = 298)	254 (85.2)	81.1–89.4
Condom use at last sex (n = 253)	183 (72.3)	64.6–80.1
Mean number of casual partners (SD) (n = 254)	23.0 (6.2)	19.8–26.3
Median (interquartile range)	10	3–30
Exchange sex partner, last 12 months (n = 299)	247 (82.6)	78.0–97.2
Condom use at last sex (n = 242)	197 (81.4)	73.8–89.1
Alcohol use at last sex (n = 245)	101 (41.2)	34.8–47.6
Mean number of exchange partners, last week (SD) (n = 247)	5.8 (19.9)	4.7–6.8
Median (interquartile range)	3	0–7
Ever used cocaine (n = 304)	100 (32.9)	25.0–39.8
Ever used crack cocaine (n = 304)	21 (6.9)	2.5–11.4
High-risk cocaine use (≥1/week for ≥25 days in last six months, n = 304)	89 (29.3)	23.4–35.1
Partner of unknown HIV status, last six months (n = 290)	254 (87.6)	82.3–92.9
Condomless sex with unknown status partner (n = 286)	158 (44.8)	35.6–53.9
Tested for HIV ever (n = 296)	284 (95.9)	93.9–98.0
Tested in the last six months (n = 284)	239 (84.2)	79.7–88.6
Knows where to get a free condom (n = 301)	276 (91.7)	88.5–94.9
Ever approached by an HIV prevention outreach worker (n = 301)	268 (89.0)	84.6–93.5
Received a condom from an HIV prevention program last 12 months (n = 301)	276 (91.7)	87.4–96.0

^aAdjusted for sampling design.

Sexual and substance use behaviors are also shown in Table 2. More than half had sex before the age of 15 (58.9%). More than one-third (35.2%) reported they had a stable partner and 39.3% of those used condoms with their stable partner last time they had sex. Most trans women had a casual partner in the last six months (85.2%) or an exchange partner (82.6%). The mean number of casual partners in the last six months was 23, and 72.3% used condoms during sex with their last casual partner. The mean number of exchange partners in the last week was 5.8, and 81.4% used condoms with their last exchange partner. Two-fifths (41.2%) used alcohol before the last time they had sex with an exchange partner. Almost one-third ever used cocaine (32.9%) and 29.2% were classified as high-risk cocaine users. Close to half (44.8%) had condomless sex with a partner of unknown HIV status.

Engagement in HIV prevention activities was high. The vast majority of participants had been previously tested for HIV (95.9%), most of whom had been tested in the last six months (84.2%). Most knew where to get a free condom (91.7%) and had been given one by a HIV prevention program in the last year (91.7%).

HIV prevalence rapidly increased with age. While no infections were detected among trans women in the 15–19 year-old group, HIV prevalence was 9.5% among trans women ages 20–24 years old, increasing to 39.6% among 30–34 year olds before peaking at 42.1% among trans women age 35–39 years.

Table 3 shows significant associations with HIV infection. HIV increased with age (adjusted OR [AOR] 1.06 per year, 95% CI 1.03–1.10). Those residing in Asunción department had higher odds of HIV infection (AOR 4.75, 95% CI 1.57–14.36). Moreover, high-risk cocaine use was associated with higher odds of infection (AOR 1.11–3.95).

Table 3.

Correlates of HIV infection among transgender women, Paraguay, 2017 (N = 304).

Correlate	Adjusted odds ratio (95% confidence interval)^a	p-value
Age (per year)	1.06 (1.03–1.10)	<0.001
Reside in Asunción department	4.75 (1.57–14.36)	0.007
High-risk cocaine use	2.09 (1.11–3.95)	0.024

^aAdjusted for sampling design.

Discussion

Paraguay joins an increasing number of countries around the world to find trans women as the population at highest risk for HIV.¹ Once studies specifically define trans women as distinct from MSM and develop sampling strategies to reach them, their highest level of HIV prevalence becomes evident. In Paraguay, we found one in four trans women were living with HIV. This compares to an HIV prevalence of 0.3% among adult women and 0.6% among adult men in the general population, and even higher than the estimated 15.4% among MSM, and 7% among FSWs in 2018.¹⁷ Our data also suggest that HIV prevalence rises from 0% among teenage trans women to 9.5% between the ages of 20 and 24 years, indicating a very high incidence in these few years. High HIV incidence continues through the late 20s and 30s, exceeding 40% before age 40 years. A similar pattern was seen in San Francisco,¹⁸,¹⁹ Rio de Janeiro,³ São Paulo,²⁰ Peru,¹,⁴ Cambodia,²¹ and Montevideo.²²

In addition to age, our study also found residing in Asunción department and frequent cocaine use associated with HIV infection. Asunción department is the most urban in Paraguay and attracts internal migrants throughout the country who are often unemployed. Notably, over half of trans women in our survey did not complete secondary education. Although not directly measured in our brief survey, trans women in Paraguay’s risk for HIV may be predicated on their social marginalization leading to low educational and employment opportunities creating the need for behaviors to ensure their survival, as in other parts of the world including Latin America.¹²,¹³,²³,²⁴ We found that trans women in Paraguay had a large number of recent sexual partners, including exchange partners to meet their basic needs. These conditions are likely to result in highly interconnected sexual networks and partner concurrency. Concurrency may also include more stable partners, reported by one-third of trans women in our survey. Moreover, prior research with trans women finds that condomless sex is most common among trans women in main partnerships.²⁵ Prevention efforts should consider prioritizing trans women and their main partners for interventions to enhance safer sexual agreements and for partner HIV testing.

On the positive side, we found evidence that trans women are engaged in HIV prevention. Over 80% of participants living with HIV reported being previously diagnosed, over 95% had been tested for HIV, with nearly four-fifths of those having tested in the last six months. Contact with prevention outreach education and free condom distribution were also high. These findings are welcome news in light of a recent ministerial-level resolution in Paraguay that providers call trans women by their chosen social name and pronoun. However, the resolution falls only within the scope of the Ministry of Public Health. The Ministry of Public Health has also built a cadre of trained peer promoters to distribute condoms, provide education, and link trans women to health services. Despite progress on meeting the health care needs and rights of trans women in Paraguay, trans women, especially those engaging in sex work on the streets, remain vulnerable to violence.

We recognize that a primary limitation of our study is how representative the sample is of trans women in Paraguay. A gold standard population-based sampling design is not yet possible for trans women in the context of Paraguay. In the absence of a national census that records transgender status, it is not possible to assess how representative our sample is of the whole population of trans women in our country. The sample was also selected to include five departments that are more densely inhabited than much of the rest of the country. Our sample does not represent the experiences of trans women in more rural areas. We anticipate that our sample may over-represent trans women who are visible in venues where sex work occurs and who access HIV prevention programs. These biases may arise from our sampling design which began with venue mapping, outreach worker community guides, and service provider client rosters. The tendency toward venue visibility may over-estimate the prevalence of sex work in the population and subsequently HIV prevalence. We also note a similar bias may pertain to the high level of exposure to prevention programs, including HIV testing, in the sample. This bias may therefore over-estimate the proportion of trans women with HIV who were previously diagnosed. There is also the potential for participation bias. We did not record how many trans women approached declined to be screened for eligibility or declined participation if eligible. The impact of this potential participation bias is unknown.

We also recognize uncertainties in the statistical approach to analyze the data obtained by our hybrid sampling design.¹⁵ The present report treats the data as starting from a simple random sample of venues and clients with adjustment of the standard errors using the randomly selected venue or client as a single-stage sampling unit, with 61 units in the present case. We acknowledge this is a simplification as further recruitment of peers stems from these initial random primary sampling units with uncertain probability. Probability weights to adjust point estimates would require assumptions on the relative probabilities of inclusion that are difficult to measure and verify. Nonetheless, the effects may be mitigated by a small average peer-recruited cluster size and many small clusters. Even when taking these uncertainties into consideration, we believe there is little doubt that the prevalence of HIV is high among trans women in Paraguay. This conclusion is bolstered by the consistency of our study with the number of known HIV cases in care and the relatively small population size. Moreover, our findings are consistent with the available data from other parts of the world, especially in Latin America.¹,³,²⁰,²²,²⁶ Finally, the interviewer-administered mode for the questionnaire raises the possibility of social desirability response bias.

Despite limitations, our data are a starting point to advocate for HIV prevention programs tailored for trans women apart from MSM, especially for those in urban areas, in their 20s, and include addressing cocaine use. Programs to deliver effective prevention, such as pre-exposure prophylaxis (PrEP), should prioritize trans women with increased availability in Paraguay. Willingness to use PrEP among trans women in neighboring Brazil has been shown to be high²⁷; future research will need to assess willingness to use and barriers to its use in Paraguay. As is often the case with research, our study raises questions that our cross-sectional design cannot answer. Longitudinal studies are needed to know if the apparent high level of transmission continues to the present and to identify risk factors for seroconversion. Another unanswered question is which partners are the source of infection among trans women. Studies of the partners of trans women may be the key to understanding how trans women reached the highest level of prevalence of any population in Paraguay and or other countries. Interventions to address partners and cocaine use among trans women may be an important starting point for targeted prevention that meets the needs of this under-serviced population.

Footnotes

Acknowledgments

Preliminary findings of this study were presented at the IUSTI 2018 World + European Congress, 24–29 June 2018, Dublin, Ireland, accessible at: .

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by The Global Fund (grant no. PRY-H-CIRD).

ORCID iDs

Gloria Aguilar

Willi McFarland

References

Baral

Poteat

Stromdahl

, et al. Worldwide burden of HIV in transgender women: a systematic review and meta-analysis. Lancet Infect Dis 2013; 13: 214–222.

Silva-Santisteban

Eng

de la Iglesia

, et al. HIV prevention among transgender women in Latin America: implementation, gaps and challenges. J Int AIDS Soc 2016; 19: 20799.

Grinsztejn

Jalil

Monteiro

, et al. Unveiling of HIV dynamics among transgender women: a respondent-driven sampling study in Rio De Janeiro, Brazil. Lancet HIV 2017; 4: e169–e176.

Silva-Santisteban

Raymond

Salazar

, et al. Understanding the HIV/AIDS epidemic in transgender women of Lima, Peru: results from a sero-epidemologic study using respondent-driven sampling. AIDS Behav 2012; 16: 872–881.

Nemoto

Bodeker

Iwamoto

, et al. Practices of receptive and insertive anal sex among transgender women in relation to partner types, sociocultural factors, and background variables. AIDS Care 2014; 26: 434–440.

Reisner

Poteat

Keatley

, et al. Global health burden and needs of transgender populations: a review. Lancet 2016; 388: 412–436.

Herbst

Jacobs

Finlayson

, et al. Estimating HIV prevalence and risk behaviors of transgender persons in the United States: a systematic review. AIDS Behav 2008; 12: 1–17.

Rowe

Santos

McFarland

, et al. Prevalence and correlates of substance use among trans female youth ages 16–24 years in the San Francisco Bay area. Drug Alcohol Depend 2015; 147: 160–166.

Brookfield

Dean

Forrest

, et al. Barriers to accessing sexual health services for transgender and male sex workers: a systematic qualitative meta-summary. AIDS Behav 2020; 24: 682–696.

10.

Wilson

Garofalo

Harris

, et al. Transgender female youth and sex work: HIV risk and a comparison of life factors related to engagement in sex work. AIDS Behav 2009; 13: 902–913.

11.

Poteat

Scheim

Xavier

, et al. Global epidemiology of HIV infection and related syndemics affecting transgender people. J Acquir Immune Defic Syndr 2016; 72: S210–S219.

12.

Brennan

Kuhns

Johnson

, et al. Syndemic theory and HIV-related risk among young transgender women: the role of multiple, co-occurring health problems and social marginalization. Am J Public Health 2012; 102: 1751–1757.

13.

Shannon

Crago

Baral

, et al. The global response and unmet actions for HIV and sex workers. Lancet 2018; 392: 698–710.

14.

Aguayo

Laguna-Torres

Villafane

, et al. Epidemiological and molecular characteristics of HIV-1 infection among female commercial sex workers, men who have sex with men and people living with AIDS in Paraguay. Rev Soc Bras Med Trop 2008; 41: 225–231.

15.

Raymond

Chen

McFarland

“ Starfish sampling”: a novel, hybrid approach to recruiting hidden populations. J Urban Health 2019; 96: 55–62.

16.

Kendall

Kerr

Gondim

, et al. An empirical comparison of respondent-driven sampling, time location sampling, and snowball sampling for behavioral surveillance in men who have sex with men, Fortaleza, Brazil. AIDS Behav 2008; 12: S97–S104.

17.

UNAIDS. Country factsheets, Paraguay, https://www.unaids.org/en/regionscountries/countries/paraguay (2018, accessed 8 May 2020).

18.

Wilson

Chen

Arayasirikul

, et al. Differential HIV risk for racial/ethnic minority trans*female youths and socioeconomic disparities in housing, residential stability, and education. Am J Public Health 2015; 105: e41–e47.

19.

Baguso

Turner

Santos

, et al. Successes and final challenges along the HIV care continuum with trans women in San Francisco. J Int AIDS Soc 2019; 22: e25270.

20.

Veras

Cezaretto

Deus

, et al. Trans incarceration experiences, cycle of violence and increased risk of HIV infection: results from Muriel Project, Sao Paulo, Brazil. In: Annual meeting of the International AIDS Society, Durban, South Africa, 2016.

21.

Weissman

Ngak

Srean

, et al. HIV prevalence and risks associated with HIV infection among transgender individuals in Cambodia. PLoS One 2016; 11: e0152906.

22.

Russi

Serra

Viñoles

, et al. Sexual transmission of hepatitis B virus, hepatitis C virus, and human immunodeficiency virus type 1 infections among male transvestite commercial sex workers in Montevideo, Uruguay. Am J Trop Med Hyg 2003; 68: 716–720.

23.

Colchero

Cortés-Ortiz

Romero-Martínez

, et al. HIV prevalence, sociodemographic characteristics, and sexual behaviors among trans women in Mexico city. Salud Publica Mex 2015; 57: s99–s106.

24.

Costa

Fontanari

Jacinto

, et al. Population-based HIV prevalence and associated factors in male-to-female transsexuals from Southern Brazil. Arch Sex Behav 2015; 44: 521–524.

25.

Wilson

Santos

Raymond

HF.

Sexual mixing and the risk environment of sexually active transgender women: data from a respondent-driven sampling study of HIV risk among trans women in San Francisco, 2010. BMC Infect Dis 2014; 14: 430.

26.

Ortiz-Martínez

Ríos-González

CM.

Need for more research on and health interventions for transgender people. Sex Health 2017; 14: 196–197.

27.

Jalil

Grinsztejn

Velasque

, et al. Awareness, willingness, and PrEP eligibility among transgender women in Rio De Janeiro, Brazil. J Acquir Immune Defic Syndr 2018; 79: 445–452.