Download as pdf or txt
Download as pdf or txt
You are on page 1of 8

Articles

Unveiling of HIV dynamics among transgender women:


a respondent-driven sampling study in Rio de Janeiro, Brazil
Beatriz Grinsztejn*, Emilia M Jalil*, Laylla Monteiro, Luciane Velasque, Ronaldo I Moreira, Ana Cristina F Garcia, Cristiane V Castro, Alícia Krüger,
Paula M Luz, Albert Y Liu, Willi McFarland, Susan Buchbinder, Valdilea G Veloso, Erin C Wilson, for the Transcender Study Team†

Summary
Background The burden of HIV in transgender women (transwomen) in Brazil remains unknown. We aimed to estimate Lancet HIV 2017
HIV prevalence among transwomen in Rio de Janeiro and to identify predictors of newly diagnosed HIV infections. Published Online
February 7, 2017
http://dx.doi.org/10.1016/
Methods We recruited transwomen from Rio de Janeiro, Brazil, by respondent-driven sampling. Eligibility criteria
S2352-3018(17)30015-2
were self-identification as transwomen, being 18 years of age or older, living in Rio de Janeiro or its metropolitan area,
See Online/Comment
and having a valid peer recruitment coupon. We recruited 12 seed participants from social movements and formative http://dx.doi.org/10.1016/
focus groups who then used peer recruitment coupons to refer subsequent peers to the study. We categorised S2352-3018(17)30014-0
participants as HIV negative, known HIV infected, or newly diagnosed as HIV infected. We assessed predictors of *Contributed equally
newly diagnosed HIV infections by comparing newly diagnosed with HIV-negative participants. We derived †Members listed at the end of
population estimates with the Respondent-Driven Sampling II estimator. the Article
Evandro Chagas National
Findings Between Aug 1, 2015, and Jan 29, 2016, we enrolled 345 eligible transwomen. 29·1% (95% CI 23·2–35·4) of Institute of Infectious Diseases,
Oswaldo Cruz Foundation,
participants had no previous HIV testing (adjusted from 60 participants), 31·2% (18·8–43·6) had HIV infections
Rio de Janeiro, Brazil
(adjusted from 141 participants), and 7·0% (0·0–15·9) were newly diagnosed as HIV infected (adjusted from (B Grinsztejn MD, E M Jalil MD,
40 participants). We diagnosed syphilis in 28·9% (18·0–39·8) of participants, rectal chlamydia in 14·6% (5·4–23·8), L Monteiro BPd, R I Moreira BSc,
and gonorrhoea in 13·5% (3·2–23·8). Newly diagnosed HIV infections were associated with black race (odds ratio 22·8 A C F Garcia MD, C V Castro BS,
P M Luz PhD, V G Veloso MD);
[95% CI 2·9–178·9]; p=0·003), travesti (34·1 [5·8–200·2]; p=0·0001) or transsexual woman (41·3 [6·3–271·2]; p=0·0001)
Federal University of the State
gender identity, history of sex work (30·7 [3·5–267·3]; p=0·002), and history of sniffing cocaine (4·4 [1·4–14·1]; p=0·01). of Rio de Janeiro, Rio de Janeiro,
Brazil (L Velasque PhD);
Interpretation Our results suggest that transwomen bear the largest burden of HIV among any population at risk in Department of Surveillance,
Prevention and Control of
Brazil. The high proportion of HIV diagnosis among young participants points to the need for tailored long-term Sexually Transmitted Diseases,
health-care and prevention services to curb the HIV epidemic and improve the quality of life of transwomen in Brazil. Aids and Viral Hepatitis,
Brazilian Ministry of Health,
Funding Brazilian Research Council, National Institute of Allergy and Infectious Diseases, Brazilian Sexually Brazil (A Krüger BPharm); Bridge
HIV, San Francisco Department
Transmitted Disease/AIDS, and Viral Hepatitis Department of the Brazilian Ministry of Health. of Public Health, San Francisco,
CA, USA (A Y Liu MD,
Introduction sampling (RDS) study of transwomen in Rio de Janeiro, S Buchbinder MD,
Of all populations affected by HIV, evidence suggests Brazil. This is the second largest city in Brazil and E C Wilson DrPH); Departments
of Medicine, Epidemiology and
that transgender women (transwomen) might carry the the state capital, with the second largest number of Biostatistics, University of
heaviest HIV burden worldwide.1 To date, investigators HIV/AIDS cases reported in the country compared with California, San Francisco,
of several studies2 have found rates of HIV infection other cities.6 We aimed to establish point estimates for San Francisco, CA, USA
among transwomen that are substantially higher than the prevalence of HIV and other sexually transmitted (W McFarland MD, S Buchbinder)

are those among other groups at risk. Authors of a diseases (STDs) among transwomen and to identify Correspondence to:
Dr Beatriz Grinsztejn, Evandro
meta-analysis1 of pooled data among transwomen from predictors of newly diagnosed HIV infections. Chagas National Institute of
ten low-income countries found an HIV prevalence of Infectious Diseases, Oswaldo
18% and a 50-times increased odds of HIV infection Methods Cruz Foundation, Rio de Janeiro
compared with other adults of reproductive age. Study design and population 21040-360, Brazil
gbeatriz@ini.fiocruz.br
Investigators of population-based studies3 of transwomen We use transwomen as an umbrella term that includes
in South America have documented HIV prevalences as travestis, transsexual women, and other people with a
high as 30%. Investigators of a cross-sectional study4 of gender identity different from that typically associated
284 transwomen seeking sex reassignment surgery in with their male sex assigned at birth (appendix p 2). See Online for appendix
southern Brazil (1997–2014) found 25% living with HIV. We did the study at the Oswaldo Cruz Foundation
Investigators of one Brazilian study5 of travestis done (FIOCRUZ) in Rio de Janeiro, Brazil. We used RDS, an
in 2008 found that 12% self-reported having HIV. established method to obtain robust and diverse samples
Rigorous population-based HIV prevalence and of populations with high susceptibility to HIV,7–9 because
incidence studies of transwomen are needed to support no sampling frame exists for transwomen. A purported
development of public health policies tailored to this benefit of RDS is that estimates of the true population
highly vulnerable population. In an attempt to address can be derived with use of statistical weights for creation
this gap, we did Transcender, a respondent-driven of unbiased prevalence estimates.

www.thelancet.com/hiv Published online February 7, 2017 http://dx.doi.org/10.1016/S2352-3018(17)30015-2 1


Articles

Research in context
Evidence before this study HIV-infected transgender women were not aware of their
We searched PubMed for articles published up to Sept 6, 2016, serostatuses. 43·7% of the transgender women newly
with the following search terms: (HIV OR [sexually transmitted diagnosed as HIV infected reported a negative HIV test within
diseases OR diseases, sexually transmitted]) AND prevalence AND the previous year. Newly diagnosed HIV infections were
(transgender persons OR transsexual persons). We excluded associated with black race, travesti or transgender woman
studies of populations other than transgender women (eg, men gender identity, sex work, and sniffed cocaine use. Our
who have sex with men). We identified one systematic review and findings indicate that transgender women are highly
one systematic review and meta-analysis. Four studies used vulnerable to HIV infection and that the structural context of
respondent-driven sampling and enrolled only transgender social exclusion and marginalisation surrounding trans
women. None of the studies analysed newly diagnosed infections populations might enhance their vulnerability.
as an outcome to characterise predictors of HIV acquisition. Only
Implications of all the available evidence
one study assessed syphilis status, but only with non-treponemic
The high proportion of transwomen infected with HIV, some
tests (eg, rapid plasma region). No studies assessed chlamydia
of whom were newly diagnosed and probably recently
infection and gonorrhoea. Also, none of these studies measured
infected, corroborates the urgent need for effective prevention
other biomarkers for HIV infection besides HIV rapid testing
strategies for this population, including pre-exposure
(eg, CD4 cell count, viral load, and pooled HIV RNA testing).
prophylaxis. Additionally, interventions aiming to overcome
Added value of this study stigma and discrimination against transwomen communities
Our results show that not only are HIV and sexually are essential.
transmitted disease prevalences high, but also that 7·0% of

We engaged the transwomen community throughout Rio de Janeiro or Baixada (part of the Rio de Janeiro
the development, implementation, and dissemination metropolitan area), and possessed a valid peer recruitment
of this project. We convened four focus group coupon.
discussions with 34 transwomen to vet the naming The Evandro Chagas National Institute of Infectious
of the project, to determine appropriate language related Diseases-FIOCRUZ Institutional Review Board provided
to gender identity for the survey instrument, and to ethical approval for this project. All participants signed
ensure that all study procedures were sensitive to the informed consent forms before study procedures began.
needs of participants. Three members of the community All procedures were approved by the local ethics
were part of the study team in charge of study committee and linkage is part of the Evandro Chagas
implementation. Once we had analysed study data, we National Institute of Infectious Diseases-FIOCRUZ HIV
convened a community town hall to discuss study results Clinical Cohort’s regular data checking procedures.
with the trans community members. We also addressed All data that can identify participants are kept in
strategies and challenges related to dissemination of password-protected files encrypted with a strong algorithm
study results to the trans community outside those (AES-256). The files have highly restricted access by
present at the town hall. We refined and wrote analyses personnel involved in the data analyses procedures.
with trans community input.
On the basis of formative focus group findings, we Procedures
selected 12 so-called seed participants to ensure that the The three recruitment RDS assumptions were met for
sample was not over-represented by key variables (eg, age, this study11 (ie, population members knew each other as
race or ethnicity, trans identities, education, geography, members of the trans population; participants were well
HIV status, history of sex work, and risk behaviours). networked, as evidenced by long recruitment chains
Participants received up to five coupons that were used achieving cross-recruitment and equilibrium; and the
to refer peers to the study until the sample size was sample is probably small relative to the overall trans
reached and equilibrium was achieved on key variables. population). Incentives for study participation consisted
Equilibrium was reached when the sample composition of snacks, sexual health materials, make-up, a medical
from one wave to the next differed by less than 2%.10 visit, and transportation reimbursement. We scheduled
We specifically monitored education, geography, race or this medical visit after study enrolment. We immediately
ethnicity, sex work status, and HIV status between offered all participants who tested positive for HIV
waves to ensure equilibrium was reached. We included linkage to care, specialised HIV care, and combination
participants according to the inclusion and exclusion antiretroviral therapy. We provided treatment for any
criteria only, and we did not modify these criteria on the diagnosed STD as well as hepatitis B vaccination for
basis of equilibrium assessments. Individuals were those who needed it. We referred participants with
eligible for the study if they self-identified as transwomen, hepatitis B or C to specialised care at FIOCRUZ
were 18 years of age or older, reported living in (appendix p 2).

2 www.thelancet.com/hiv Published online February 7, 2017 http://dx.doi.org/10.1016/S2352-3018(17)30015-2


Articles

All surveys were done face-to-face by trained groups to be significantly different from each other
interviewers with data input into computers. The survey (appendix pp 2–3). Accordingly, to study the predictors
instrument captured sociodemographic information, of HIV acquisition, we used a subset of the original
sexual behaviour, gender transition procedures and dataset that excluded the known HIV-infected group and
hormone use, discrimination and violence, alcohol and compared those who were newly HIV-diagnosed with
drug use, physical and mental health, history of STDs, the HIV-negative group. The modelling process included
HIV testing history, HIV care information, and HIV stepwise backward logistic regression including all
prevention knowledge. variables with p values of less than 0·20 in univariate
We did HIV testing following the Brazilian Ministry of modelling, removing terms of greatest non-significance
Health algorithm.12 We did a different rapid test if the first until a final model was reached where all variables had a
test (HIV Strip Test; Bioeasy, Hagal-dong, Giheung-gu, p value of less than or equal to 0·05. We used the RDS
Yongin-si, Gyeonggi-do, South Korea) was positive. If the Analysis Tool (version 6.0) to examine homophily, mean
second test (Abon HIV Test; Abon, Hangzhou, China) was network size, waves of recruitment, crude sample
positive, we considered individuals HIV positive; if the stability by week of recruitment, and equilibrium by
second test was negative, we considered individuals wave of recruitment. We used the RDSII estimator to
indeterminate and did serology (ELISA HIV test). We weight and adjust population estimates according to
considered individuals with a first negative test HIV recruitment patterns. We did weighted, bivariate, and
negative. Additionally, we offered participants with a multivariate analysis with RDS Analyst Software
negative HIV rapid test who reported condomless anal version 0.57.13 We used RDSII estimates, with
intercourse in the past 30 days pooled HIV RNA testing to 1000 iterations, 95% CIs for the estimates, and
diagnose acute HIV infection. All participants with a 500 bootstrap replications. As results are RDS-weighted,
positive HIV test had their HIV viral loads (real-time PCR) we provide only estimates and not absolute numbers.
and CD4 cell counts assessed. Given the very small proportion of missing data (1% for
We did Venereal Disease Research Laboratory tests for the main outcome [HIV infection]), we did not use
syphilis screening; we confirmed positive results with a imputation techniques and instead simply excluded
microhaemagglutination assay for Treponema pallidum. missing data from the modelling process.
We defined active or recent syphilis as titres of at
least 1/8 plus a positive microhaemagglutination assay Role of the funding source
for T pallidum. We used rapid tests to screen for hepatitis B The funders of the study had no role in study design,
and C. If positive, we did serology (anti-HBs, HBs data collection, data analysis, data interpretation, or
antigen, and anti-HBc for hepatitis B and anti-hepatitis C writing of the report. The corresponding author had full
virus for hepatitis C) for confirmation. We considered access to all the data in the study and had final
patients to have active hepatitis B if HBs antigen was responsibility for the decision to submit for publication.
positive. We screened for rectal Chlamydia trachomatis
and Neisseria gonorrhoeae infection with the Abbott Real Results
Time platform and the Amplification Reagent Kit for Between Aug 1, 2015, and Jan 29, 2016, 374 individuals
these organisms (Abbott Molecular, Des Plains, IL, USA). returned with a recruitment coupon, 370 (99%) consented
We repeated all indeterminate results for rectal infections and were screened, and 345 (93%) eligible transwomen
with the same tests on the same samples. All laboratory participated in the study. Recruitment was completed in
testing was processed at the FIOCRUZ laboratory.

Statistical analysis Age Known HIV Engagement Schooling Race Waves Recruits
(years) status in sex work (years) or colour (n) (n)
The minimum sample size for this study was
300 participants, enabling us to detect an estimated HIV A 30 Positive No 9–12 Black 6 42
prevalence of 5%, with 95% CI, 80% power, 5% precision, B 31 Negative Current 9–12 White 2 6
and a design effect of 2. We calculated HIV and STD C 33 Negative Current 9–12 White 4 51
prevalences on the basis of test results. For this analysis, D 37 Negative Ever (not current) 4–8 Mixed 4 11
we categorised participants as HIV negative, known HIV E 27 Negative Ever (not current) 9–12 Mixed 4 27
infected, or newly diagnosed as HIV infected. We F 36 Negative No ≥12 Black 3 12
categorised those who self-reported being HIV negative G 29 Negative No 9–12 Mixed 7 81
in the survey but tested HIV positive as newly diagnosed. H 33 Negative Current 9–12 White 4 30
To rule out any possible misreporting of HIV infection I 42 Positive Ever (not current) 9–12 Mixed 7 28
(ie, a denial of knowledge of HIV infection), we linked J 42 Positive Ever (not current) 4–8 Mixed 2 8
our data with information from the Brazilian Information K 29 Negative No ≥12 Black 6 43
Registry Databases. L 24 Negative Current ≥12 White 2 6
We used χ² tests to compare the known HIV-infected
Table 1: Seed participant characteristics
group with the newly diagnosed group and found these

www.thelancet.com/hiv Published online February 7, 2017 http://dx.doi.org/10.1016/S2352-3018(17)30015-2 3


Articles

Crude (n=345) RDS weighted Crude (n=345) RDS weighted


Age (years)* (Continued from previous column)
18–24 95 (27·5%) 30·0% (20·1–39·9) Ever had discrimination 333 (96·5%) 96·7% (91·6–100·0)
25–35 145 (42·0%) 39·9% (29·0–50·8) Ever had physical violence 187 (54·2%) 48·6% (36·6–60·6)
36–45 66 (19·1%) 17·9% (7·3–28·5) Ever been raped 164 (47·5%) 41·5% (29·0–53·9)
>45 39 (11·3%) 12·2% (4·4–19·9) Ever drug use 266 (77·1%) 75·7% (64·8–86·6)
Self-declared race or colour Sniffed cocaine 149 (43·2%) 41·5% (29·3–53·7)
White 79 (22·9%) 28·4% (25·9–30·9) Glue 86 (24·9%) 23·3% (13·4–33·3)
Mixed 175 (50·7%) 43·7% (31·8–55·7) Downers 125 (36·2%) 41·4% (28·9–53·9)
Black 84 (24·3%) 27·3% (15·0–39·6) Marijuana 203 (58·8%) 56·1% (43·6–68·6)
Other 7 (2·0%) 0·5% (0·0–3·3) Others 82 (23·8%) 23·8% (12·6–34·9)
Born in Rio de Janeiro 250 (72·5%) 58·5% (50·6–66·3) Binge drinking§ 227 (65·8%) 68·1% (56·7–79·6)
Housing instability† 149 (43·2%) 40·4% (28·0–52·9) Number of sex partners in the last 6 months*
Monthly income (US$)*‡ 0 1/325 (0·3%) 0·0% (0·0–0·0)
≤130 140/322 (43·5%) 54·7% (44·4–65·0) 1–4 93/325 (28·6%) 40·0% (40·0–50·0)
131–260 109/322 (33·9%) 22·3% (8·9–35·8) >4 231/325 (71·1%) 60·0% (50·0–60·0)
>260 73/322 (22·7%) 23·0% (10·7–35·2) Condomless anal 219 (63·5%) 68·2% (57·4–79·0)
Years of education* intercourse with last
three partners
<4 27 (7·8%) 10·1% (2·5–17·7)
Active STD
4–8 108 (31·3%) 29·6% (23·1–36·1)
Syphilis 112 (32·7%) 28·9% (18·0–39·8)
9–12 188 (54·5%) 56·3% (46·5–66·1)
Rectal chlamydia 46 (14·1%) 14·6% (5·4–23·8)
>12 22 (6·4%) 4·0% (0·0–8·4)
Rectal gonorrhoea 25 (7·6%) 13·5% (3·2–23·8)
Current gender identity
Hepatitis B 10 (2·9%) 0·7% (0·1–1·3)
Travesti 131 (38·0%) 25·6% (16·0–35·3)
Hepatitis C 6 (1·7%) 0·8% (0–1·8)
Woman 96 (27·8%) 39·2% (24·2–54·2)
HIV-positive self-reported 101 (29·3%) 24·2% (11·5–37·0)
Transsexual woman 107 (31·0%) 29·1% (18·2–40·0)
status
Other definitions 11 (3·2%) 6·1% (0·6–11·6)
HIV-positive status 141 (41·2%) 31·2% (18·8–43·6)
Changed name in identity 9 (2·6%) 1·4% (0·2–2·5) via testing
documents
Known HIV infected 101 (29·3%) 24·2% (11·5–36·9)
Sexual orientation
Newly diagnosed 40 (11·6%) 7·0% (0·0–15·9)
Heterosexual 212 (61·4%) 54·4% (40·7–68·2)
Undetectable viral load¶ 60 (43·5%) 35·4% (19·6–51·3)
Homosexual 105 (30·4%) 37·7% (23·8–51·5)
CD4 cell count*
Other definitions 28 (8·1%) 7·9% (0·0–15·8)
≤200 17 (12·6%) 8·4% (0·0–23·6)
What gender they are attracted to
201–350 14 (10·4%) 4·5% (0·0–12·3)
Only men 326 (94·5%) 93·2% (88·6–97·9)
351–500 23 (17·0%) 13·7% (1·6–25·8)
Only women 3 (0·9%) 0·6% (0·0–3·1)
>500 81 (60·0%) 73·3% (60·9–85·7)
Other 16 (4·6%) 6·2% (2·3–10·1)
Currently taking hormones 170 (52·3%) 56·8% (45·3–68·4) Data are n (%), % (95% CI), or n/N (%). Proportions are calculated for valid data;
missing data are excluded. RDS=respondent-driven sample. STD=sexually
Ever used soft tissue fillers 166 (48·1%) 32·3% (22·1–42·6)
transmitted disease. *We reclassified these continuous variables as categorical.
Ever had gender-related 20 (5·8%) 6·2% (0·9–11·4) †If the participant referred to living in a shelter, living on the streets, being allowed
surgery (vagina, penis, to live somewhere as a favour, or living at work. ‡US$1·00=R$3·85. §Defined as
or oorchiectomy) six or more alcoholic drinks on any one occasion. ¶Only transwomen on
Access to health care in the 199 (57·7%) 49·4% (38·2–60·6) combination antiretroviral therapy with a viral load of less than 40 copies per mL.
last 6 months
Table 2: Crude and weighted characteristics of study participants
Access to trans-related 51 (14·8%) 15·9% (7·7–24·2)
health care
Age at sexual debut (years)*
26 weeks with a mean of 3·6 (SD 1·6) recruitment waves
<12 121/344 (35·2%) 31·0% (19·6–42·3)
for active seeds. The number of coupons returned was
12–18 195/344 (56·7%) 62·2% (51·1–73·3)
374 (37%) of 1020 coupons distributed. The pattern of
≤19 28/344 (8·1%) 6·9% (0·0–14·1) recruitment according to HIV status is shown in the
Engagement in sex work appendix (p 4). Reasons for ineligibility were invalid
Current 167 (48·4%) 34·1% (22·8–45·4) coupon (17 individuals), non-transgender identity (seven),
Ever (not currently) 104 (30·1%) 24·5% (14·7–34·2) and residence outside Rio de Janeiro or Baixada (one).
Never 74 (21·4%) 41·5% (28·3–54·7) Moderate positive homophily was identified for HIV
(Table 2 continues in next column) status (0·27) and race or colour (0·20), suggesting a
moderate tendency to recruit others of the same HIV

4 www.thelancet.com/hiv Published online February 7, 2017 http://dx.doi.org/10.1016/S2352-3018(17)30015-2


Articles

status and race. We found a strong positive homophily for To our knowledge, this study is the largest population-
engagement in sex work (0·55), suggesting that those based study of transwomen in Brazil and one of the
with a history of sex work had the greatest tendency to largest studies in Latin America. A strength of our
recruit others like themselves. One seed (G) generated findings is that we obtained population-based estimates.
23% of our sample (table 1). Other studies of transwomen in Brazil and elsewhere
Median age was 28 years (interquartile interval 22–37; might have provided less accurate estimates of HIV
table 2). Most transwomen were living full time as a than those from this study because of convenience
woman (86·0%, 95% CI 82·0–88·0). Soft tissue fillers sampling approaches and self-reported data for HIV
were ever used by 32·3% of participants (95% CI endpoints.4,5 Moreover, our study also provided a unique
22·1–42·6) and 93·3% (86·5–100·0) accessed these opportunity to understand factors associated with new
substances outside of health facilities from unlicensed HIV infections.
individuals. Most reported ever using hormones (81·0%, We identified high STD prevalences among study
95% CI 79·0–82·0) and most used hormones without a participants. A high syphilis prevalence among Brazilian
medical prescription (87·0%, 85·0–90·0). The median transwomen sex workers has been previously described.18
number of sexual partners in the previous 6 months was To our knowledge, these data are the first to describe
eight (interquartile interval two to 50) and the mean the prevalence of anorectal chlamydia and gonorrhoea
number was 113·0 (SD 244·0). among transwomen in Brazil. High prevalences of these
Overall, 29·1% (95% CI 23·2–35·4) of transwomen
(adjusted from 60 participants) reported no previous Univariate (RDS weighted) Multivariate (RDS weighted)
HIV testing. Almost all participants agreed to be tested
OR p value OR p value
for HIV (342 [99%] participants). Among all participants,
almost a third of transwomen were estimated to be Age (years)
living with HIV, almost a quarter previously knew their 18–24 1 ·· ·· ··
HIV status, and less than 10% did not know they were 25–35 1·97 (0·44–8·84) 0·3700 ·· ··
HIV infected before participating in this study (table 2). ≥36 0·65 (0·06–6·47) 0·7190 ·· ··
Among participants with HIV infections, 22·2% Self-declared race or colour
(0·0–50·8) were not aware of their HIV status. We found
White 1 ·· 1
six participants who self-reported as HIV negative in this
Mixed or other 5·23 (0·71–38·56) 0·1039 6·2 (0·9–40·5) 0·06
study in the Brazilian Information Registry Databases
Black 6·34 (0·76–52·4) 0·0859 22·8 (2·9–178·9) 0·003
and reclassified them as known HIV infected.
Among those newly diagnosed as HIV infected, nearly Born in Rio de Janeiro 1·7 (0·5–6·2) 0·4130 ·· ··
half (48·7%, 95% CI 0·0–100·0) reported no previous Monthly income (US$)*
HIV testing and 43·7% (8·4–79·0) reported a negative ≤130 1·70 (0·34–8·35) 0·5074 ·· ··
HIV test within the past year. One participant was 131–260 6·15 (1·05–36·0) 0·0436 ·· ··
diagnosed with acute HIV infection. 44·1% (15·2–73·6) of >260 1 ·· ·· ··
transwomen newly diagnosed as HIV infected presented Years of education
with active or recent syphilis, 21·2% (0·0–51·0) presented
<4 1·33 (0·14–12·45) 0·8020 ·· ··
with rectal chlamydia, and 10·6% (0·0–47·3) presented
4–8 0·49 (0·15–1·7) 0·2610 ·· ··
with gonorrhoea. The final model shows that newly
≥9 1 ·· ·· ··
diagnosed HIV infections were associated with black race,
travesti or transsexual woman gender identity, sex work, Current gender identity
and sniffed cocaine use (table 3). Woman 1 ·· 1 ··
Travesti 21·2 (3·8–117·6) 0·0005 34·1 (5·8–200·2) 0·0001
Discussion Transsexual woman 15·3 (2·3–100·3) 0·0046 41·3 (6·3–271·2) 0·0001
Almost a third of transwomen in our study were estimated Other definitions 0·4 (0·0–6·0) 0·4826 0·2 (0·0–4·1) 0·28
to be living with HIV, which is higher than the HIV Sexual orientation
prevalence in any other key population in the Brazilian
Heterosexual 1 ·· ·· ··
HIV epidemic (4·9% for female sex workers,14 14·2% for
Homosexual 0·81 (0·20–3·33) 0·7780 ·· ··
men who have sex with men,15 5·9% for people who use
drugs,16 and 5·0% for crack users16). The HIV prevalence Other definitions 1·49 (0·19–11·4) 0·6990 ·· ··

observed in this study is also substantially higher than the Currently taking hormones 0·4 (0·1–1·7) 0·2323 ·· ··
pooled estimate for HIV among transwomen globally,1 but Ever used soft tissue fillers 2·9 (0·7–11·6) 0·1330 ·· ··
on par with that from other RDS studies of transwomen.3,17 Ever had gender-related surgery 0·07 (0·0–0·73) 0·0258 ·· ··
Our multivariate analysis showed that self-reported (vagina, penis, or oorchiectomy)
gender identity other than woman, black race, engagement Access to trans-related health care 1·29 (0·16–10·4) 0·8090 ·· ··
in sex work, and sniffed cocaine use were independently (Table 3 continues on next page)
associated with newly diagnosed HIV.

www.thelancet.com/hiv Published online February 7, 2017 http://dx.doi.org/10.1016/S2352-3018(17)30015-2 5


Articles

discrimination and stigma, which can result in increased


Univariate (RDS weighted) Multivariate (RDS weighted)
risk of HIV,22 and substance use before or during sex is
OR p value OR p value an independent predictor of condomless receptive anal
(Continued from previous page) sex in transwomen.23,24
Age at sexual debut (years) The discrepancy between self-reported HIV
<12 3·9 (0·40–39·4) 0·2340 ·· ··
prevalence (24·2%) and laboratory-confirmed HIV
(31·2%) suggests that many transwomen remain
12–18 5·26 (0·67–41) 0·1130 ·· ··
unaware of their HIV statuses. Despite higher HIV
≤19 1 ·· ·· ··
testing rates than those found among other key
Ever engaged in sex work 51·8 (6·0–450) 0·0004 30·7 (3·5–267·3) 0·002 populations in Brazil,25 29·1% had never been tested
Ever had discrimination 0·6 (0·2–1·7) 0·3410 ·· ·· for HIV before, in agreement with findings from
Ever had physical violence 7·8 (1·8–33·4) 0·005 ·· ·· another Brazilian study among transwomen.5 Reasons
Ever been raped 2·3 (0·6–9·2) 0·2460 ·· ·· for low levels of HIV testing have been described for
Ever drug use 1·5 (0·3–7·0) 0·6402 ·· ·· other key populations in Brazil.26 Fear of HIV infection,
Ever sniffed cocaine use 3·8 (1·0–14·7) 0·0560 4·4 (1·4–14·1) 0·01 stigma, and uncertain access to medical care and low
Binge drinking† 3·3 (0·9–12·0) 0·0651 ·· ··
perception of personal risk are among the cited barriers
to HIV testing.27 Without knowledge of their HIV
Five or more sex partners in the last 13·00 (2·7–61·5) 0·0013 ·· ··
6 months status, transwomen cannot benefit from early
Condomless anal intercourse with 0·3 (0·1–1·2) 0·0782 ·· ··
treatment, which is universally available at no cost for
last three partners all individuals with HIV infections in Brazil through
Current syphilis, rectal chlamydia, 2·5 (0·7–9·9) 0·1790 ·· ·· the public health system. Moreover, we found that more
or gonorrhoea than 40% of transwomen newly diagnosed as HIV
infected had a negative HIV test in the previous year.
Data in parentheses are 95% CIs. Analysis considering a subset of the original dataset of only the newly HIV-diagnosed
and HIV-negative groups. RDS=respondent-driven sampling. OR=odds ratio. *US$1·00=R$3·85. †Defined as six or
These results suggest that, had pre-exposure
more alcoholic drinks on any one occasion. prophylaxis been available during the year before the
study, then these HIV infections could have been
Table 3: Predictors of newly diagnosed HIV infection compared with being HIV negative
averted, as well as future infections derived from them.
Studies are needed to better understand than at present
infections were also found among transwomen in Peru.19 transwomen’s motivations to get tested for HIV and
Since most chlamydial infections are asymptomatic and their perception about the meaning of a negative HIV
potentially facilitate HIV acquisition and transmission,20 test result and its implications for HIV prevention.
the high prevalence of anorectal chlamydia infection Efforts to enable this vulnerable population to access
could be a contributing factor to the ongoing HIV HIV prevention interventions are of utmost importance.
epidemic in transwomen in our setting. Unfortunately, Sociostructural factors play a major part in risk of HIV
STD molecular screening is not standard of care in among transwomen. Our findings for gender are
Brazil, with diagnosis relying mostly on the syndromic interesting and comparable with those from other
approach. In the absence of symptoms, infected indi- studies. We found that transwomen who self-identified
viduals are not prompted to seek health services or to as travesti or transsexual were more likely to be newly
adjust risk practices. This population could highly diagnosed with HIV than were those who self-identified
benefit from molecular STD screening, although the as women. Transgender gender identity was also a
high cost to implement such testing suggests that these significant factor associated with HIV infection in
strategies might not be affordable in low-income and San Francisco, CA, USA.17 Transwomen suffer inordinate
middle-income settings. Cost-effectiveness analysis discrimination and violence because they are seen as
could help address the economic value of molecular transgressing gender norms.28 Discrimination and
STD testing for transwomen in these settings. violence related to gender identity are key factors
Individual-level risks are necessary for the spread explaining why transwomen have higher rates of mental
of HIV, but they are insufficient to explain the health disorders, substance use, and HIV than do
extraordinarily high HIV prevalence observed among non-transwomen.29 Identification as women might be a
transwomen in this study. The interplay of several marker of greater external or internal gender identity
HIV risk factors is more likely to explain the high acceptance than for transwomen because of various
population-specific HIV epidemic among transwomen factors, like the ability to use medical services to
than are individual-level risks alone. Many transwomen transition,30 thus reducing the risk of violence. In our
engaged in condomless anal sex, which could be in the setting, the ability to identify as women might confer a
context of economic survival and identity affirmation, as protective effect for HIV acquisition. The independent
investigators of other studies of transwomen have association of black race with new HIV diagnosis
described.21 Additionally, transgender people faced with suggests that transwomen of colour face unique social
multiple stigmas might use substances to cope with this and economic vulnerabilities created by the intersection

6 www.thelancet.com/hiv Published online February 7, 2017 http://dx.doi.org/10.1016/S2352-3018(17)30015-2


Articles

of gender identity stigma, racism, and transphobia. Our results help minimise the dearth of knowledge
Racial, socioeconomic, and gender inequalities can act about transwomen’s health and provide representative
synergistically and place people at the centre of multiple data for transwomen in Rio de Janeiro, Brazil. Our
stigmas, resulting in high risk of various poor social and results reinforce the structural context of social
health outcomes, including HIV.2,31,32 exclusion and marginalisation surrounding trans
Our population was also very young, especially populations, leading to a high vulnerability to HIV
compared with that in studies of transwomen in the infection. The high proportion of transwomen infected
USA.17 The young age of this sample has implications with HIV, some of whom were newly diagnosed and
for provision of long-term HIV care and the need for probably recently infected given that almost half of
prevention among youth and highlights that a new those newly diagnosed had a negative HIV test within
generation of transwomen exists bearing the burden of the previous year, corroborates the urgent need for
this preventable disease. Additionally, roughly 40% effective prevention strategies for this population,
were internal migrants. Transwomen from other including pre-exposure prophylaxis. Furthermore,
regions in the country migrate to the southeast, where these prevention strategies need to take into account
Rio de Janeiro is located, probably aiming for less the specifics of low-income and middle-income
stigma and more life opportunities than outside the countries, such as barriers to health access, high
area. The educational level of participants was lower engagement in sex work, high levels of violence, and
than among participants in a study of transwomen transphobia. HIV prevention strategies should be
described in Lima, Peru.3 Unfortunately, in this study, urgently tailored to these most-at-risk transwomen. If
we were not able to assess whether the feminisation the Joint UN Programme on HIV/AIDS 90-90-90
process and transgender-related discrimination could targets are to be achieved, access to HIV prevention and
have hampered their access to education; future studies care for all key populations, including transwomen, is
are needed. needed.37 Notwithstanding, to succeed, these efforts
Income was also lower among transwomen than was must be built on interventions aiming to reduce
the average Brazilian income,33 probably reflecting the discrimination that creates vulnerabilities within
scarcity of job opportunities for transwomen, leading to transwomen communities.
major challenges to maintain an adequate livelihood. Contributors
Therefore, in many settings, transwomen have been BG, EMJ, WM, ECW, SB, and VGV conceived the study and interpreted
forced to rely on sex work to survive, further exacerbating the findings. BG, EMJ, ECW, and VGV drafted the manuscript. LV did
the statistical analyses with aid from RIM, EMJ, and PML. LM, LV, RIM,
their risk of HIV and explaining the high proportions of ACFG, CVC, AK, and PML helped with data acquisition, interpretation
engagement in sex work in the population, similar to of the findings, and drafting the manuscript. WM, AYL, and SB were
other studies in the region3,5 and the USA.34 Although involved in revising the manuscript for important intellectual content.
condomless anal sex is more common with primary than All authors read and approved the final manuscript.
with commercial partners,2 economic pressures might Transcender Study Team
result in transwomen compromising safe sex practices Toni Araujo, Josias de Freitas, Jose Roberto Grangeiro, Carla Alves,
Luciana P Kamel, Kakau Ferreira, Biancka Fernandes, Aline Brito
for monetary incentives. Barcelos, Bruna Grinsztejn Joao, Nathalia Cardoso Rachid de Lacerda,
Our study has limitations. Whether RDS can provide Pedro Bomfim Leal, Sandro Nazer Coutinho, Theresa Ick, Gabriel Abi
unbiased estimates is unclear35 and the size of the Ramia Ismerio Madeira, Vinícius Pacheco, Elizabeth Fernandes, Nilo
network might be imprecise, thus leading to biased RDS Martinez Fernandes, Thiago da Silva Torres, Luana Monteiro Espíndola
Marins, Sandra Wagner Cardoso.
estimates.36 Although our estimates show high variability
as evidenced by the wide CIs, which is common with Declaration of interests
BG and PML have received funding from the Brazilian Research Council
RDS methodology and might also be a result of the (National Council for Scientific and Technological Development) and
sample size, the detected associations were of high Scientific Development and Research Funding Agency of the state of
magnitude and significant. Given its cross-sectional Rio de Janeiro. All other authors declare no competing interests.
design, this study does not allow inference of causality. Acknowledgments
Also, RDS hinges on networks for referral. Some This study was funded by the Brazilian Research Council (National
Council for Scientific and Technological Development [470056/2014-2]),
transwomen (eg, those with a high income or who had
National Institute of Allergy and Infectious Diseases (National Institutes
medical or social transition) might be under-represented of Health [UM1AI069496]), Brazilian Sexually Transmitted Disease/
since they might have small or inexistent networks AIDS, and Viral Hepatitis Department of the Brazilian Ministry of
within the transwomen population, and so our results Health. We acknowledge all of the Transcender team and participants.
We thank the ELSA-Brasil Fiocruz team members for their invaluable
might not be generalisable to them. Additionally, our
support in providing the space and warm environment for carrying out
data refer only to Rio de Janeiro and its metropolitan of the study. We thank Congressman Jean Wyllis de Matos Santos and
area, so generalisation of our results to other Brazilian Alessandra Ramos for their invaluable support. We thank Lucia Helena
cities is beyond the scope of this study. Finally, this Cardoso, Ricardo Henrique de Souza, Lais de Aguiar Faria, Denise de
Oliveira Sigales, Cristina de Oliveira Nogueira, Monica Derrico Pedrosa,
analysis did not assess variables such as stigma and and Amilton Xavier Jr for invaluable logistical support. We thank
racism that might substantially contribute to the HIV Cristina Pimenta for her support. We thank Eduarda Grinsztejn for her
epidemic in transwomen. thorough review and edits of the manuscript.

www.thelancet.com/hiv Published online February 7, 2017 http://dx.doi.org/10.1016/S2352-3018(17)30015-2 7


Articles

References 20 Centers for Disease Control and Prevention. Sexually transmitted


1 Baral SD, Poteat T, Strömdahl S, Wirtz AL, Guadamuz TE, Beyrer C. diseases treatment guidelines, 2015. MMWR Recomm Rep 2015;
Worldwide burden of HIV in transgender women: a systematic 64: 15–17.
review and meta-analysis. Lancet Infect Dis 2013; 13: 214–22. 21 Nuttbrock LA, Hwahng SJ. Ethnicity, sex work, and incident
2 Poteat T, Scheim A, Xavier J, Reisner S, Baral S. Global epidemiology HIV/STI among transgender women in New York City: a three year
of HIV infection and related syndemics affecting transgender people. prospective study. AIDS Behav 2016; published online Aug 8.
J Acquir Immune Defic Syndr 2016; 72 (suppl 3): S210–19. DOI:10.1007/s10461-016-1509-4.
3 Silva-Santisteban A, Raymond HF, Salazar X, et al. 22 Tebbe EA, Moradi B. Suicide risk in trans populations: an application
Understanding the HIV/AIDS epidemic in transgender women of of minority stress theory. J Couns Psychol 2016; 63: 520–33.
Lima, Peru: results from a seroepidemiologic study using 23 Nemoto T, Operario D, Keatley J, Han L, Soma T. HIV risk
respondent driven sampling. AIDS Behav 2012; 16: 872–81. behaviors among male-to-female transgender persons of color in
4 Costa AB, Fontanari AM, Jacinto MM, et al. Population-based HIV San Francisco. Am J Public Health 2004; 94: 1193–99.
prevalence and associated factors in male-to-female transsexuals 24 Weissman A, Ngak S, Srean C, Sansothy N, Mills S, Ferradini L.
from southern Brazil. Arch Sex Behav 2015; 44: 521–24. HIV prevalence and risks associated with HIV infection among
5 Martins TA, Kerr LR, Macena RH, et al. Travestis, an unexplored transgender individuals in Cambodia. PLoS One 2016;
population at risk of HIV in a large metropolis of northeast Brazil: 11: e0152906.
a respondent-driven sampling survey. AIDS Care 2013; 25: 606–12. 25 Brito AM, Kendall C, Kerr L, et al. Factors associated with low levels
6 Ministério da Saúde. Boletim Epidemiológico. HIV. AIDS. Brazil: of HIV testing among men who have sex with men (MSM)
Ministério da Saúde, 2016. in Brazil. PLoS One 2015; 10: e0130445.
7 Heckathorn DD. Respondent-driven sampling II: deriving valid 26 Joint UN Programme on HIV/AIDS. Global AIDS response progress
population estimates from chain-referral samples of hidden reporting 2014. Construction of core indicators for monitoring the
populations. Social Problems 2002; 49: 11–34. 2011 United Nations political declaration on HIV and AI. Geneva:
8 Heckathorn DD. Respondent-driven sampling: a new approach to Joint United Nations Programme on HIV/AIDS, 2014.
the study of hidden populations. Social Problems 1997; 44: 174–99. 27 Grant RM, Smith DK. Integrating antiretroviral strategies for
9 Heckathorn DD. Extensions of respondent-driven sampling: human immunodeficiency virus prevention: post- and pre-exposure
analyzing continuous variables and controlling for differential prophylaxis and early treatment. Open Forum Infect Dis 2015; 2: 1–7.
recruitment. Sociol Methodol 2007; 37: 151–207. 28 Lombardi EL, Wilchins RA, Priesing D, Malouf D. Gender violence:
10 Wejnert C, Heckathorn D. Web-based network sampling: transgender experiences with violence and discrimination.
efficiency and efficacy of respondent-driven sampling for online J Homosex 2001; 42: 89–101.
research. Soc Methods Res 2008; 37: 105–34. 29 Mayer KH, Grinsztejn B, El-Sadr WM. Transgender people and HIV
11 Lansky A, Drake A, Wejnert C, Pham H, Cribbin M, prevention: what we know and what we need to know, a call to action.
Heckathorn DD. Assessing the assumptions of respondent-driven J Acquir Immune Defic Syndr 2016; 72: S207–09.
sampling in the national HIV Behavioral Surveillance System 30 Wilson EC, Chen YH, Arayasirikul S, Wenzel C, Raymond HF.
among injecting drug users. Open AIDS J 2012; 6: 77–82. Connecting the dots: examining transgender women’s utilization of
12 Ministério da Saúde. Manual Técnico Para o Diagnóstico da transition-related medical care and associations with mental health,
Infecção Pelo HIV. Brazil: Ministério da Saúde, 2013. substance use, and HIV. J Urban Health 2015; 92: 182–92.
13 Handcock MS, Fellows IE, Gile KJ. 2014. RDS Analyst: software for 31 Chor D. Health inequalities in Brazil: race matters. Cad Saude Publica
the analysis of respondent-driven sampling data, version 0.42. 2013; 29: 1272–75.
http://hpmrg.org (accessed Nov 18, 2016). 32 Sevelius JM. Gender affirmation: a framework for conceptualizing
14 Szwarcwald CL, de Souza Júnior PR, Damacena GN, Junior AB, risk behavior among transgender women of color. Sex Roles 2013;
Kendall C. Analysis of data collected by RDS among sex workers in 68: 675–89.
10 Brazilian cities, 2009: estimation of the prevalence of HIV, 33 Instituto Brasileiro de Geografia e Estatística. Diretoria de Pesquisas,
variance, and design effect. J Acquir Immune Defic Syndr 2011; Coordenação de Trabalho e Rendimento, Pesquisa Nacional por
57 (suppl 3): S129–35. Amostra de Domicílios 2007/2014. http://brasilemsintese.ibge.gov.
15 Kerr LR, Mota RS, Kendall C, et al, for the HIVMSM Surveillance br/trabalho/rendimento-de-todos-os-trabalhos.html
Group. HIV among MSM in a large middle-income country. AIDS (accessed Nov 27, 2016).
2013; 27: 427–35. 34 Herbst JH, Jacobs ED, Finlayson TJ, et al. Estimating HIV
16 Ministério da Saúde. Pesquisa Nacional Sobre o Uso de Crack. prevalence and risk behaviors of transgender persons in
Brazil: Ministério da Saúde, 2014. the United States: a systematic review. AIDS Behav 2008; 12: 1–17.
17 Rapues J, Wilson EC, Packer T, Colfax GN, Raymond HF. 35 McCreesh N, Frost SD, Seeley J, et al. Evaluation of
Correlates of HIV infection among transfemales, San Francisco, 2010: respondent-driven sampling. Epidemiology 2012; 23: 138–47.
results from a respondent-driven sampling study. Am J Public Health 36 Brignol SM, Dourado I, Amorim LD, Miranda JG, Kerr LR.
2013; 103: 1485–92. Social networks of men who have sex with men: a study of
18 Grandi JL, Goihman S, Ueda M, Rutherford G. HIV infection, recruitment chains using respondent driven sampling in
syphilis, and behavioral risks in Brazilian male sex workers. Salvador, Bahia State, Brazil. Cad Saude Publica 2015;
AIDS Behav 2000; 4: 129–35. 31 (suppl 1): S170–81.
19 Leon SR, Segura ER, Konda KA, et al. High prevalence of 37 Dehne KL, Dallabetta G, Wilson D, et al. HIV prevention 2020:
Chlamydia trachomatis and Neisseria gonorrhoeae infections in anal a framework for delivery and a call for action. Lancet HIV 2016;
and pharyngeal sites among a community-based sample of men 3: e323–32.
who have sex with men and transgender women in Lima, Peru.
BMJ Open 2016; 6: e008245.

8 www.thelancet.com/hiv Published online February 7, 2017 http://dx.doi.org/10.1016/S2352-3018(17)30015-2

You might also like