Available via license: CC BY 4.0
Content may be subject to copyright.
Page 1/17
Incidence and Time-Varying Predictors of HIV and
Sexually Transmitted Infections Among Male Sex
Workers in Mexico City
Karla Ganley
Columbia University https://orcid.org/0000-0003-4872-1053
Marta Wilson-Barthes
Brown University School of Public Health
Andrew R. Zullo
Brown University School of Public Health
Sandra G. Sosa-Rubí
Instituto Nacional de Salud Publica
Carlos J. Conde-Glez
Instituto Nacional de Salud Publica
Santa García-Cisneros
Instituto Nacional de Salud Publica
Mark N. Lurie
Brown University School of Public Health
Brandon D.L. Marshall
Brown University School of Public Health
Don Operario
Brown University School of Public Health
Kenneth H. Mayer
Fenway Institute
Omar Galarraga ( omar_galarraga@brown.edu )
Brown University https://orcid.org/0000-0002-9985-9266
Research article
Keywords: male sex workers, men who have sex with men, HIV/STI transmission, risk factors, Mexico
DOI: https://doi.org/10.21203/rs.3.rs-51080/v1
License: This work is licensed under a Creative Commons Attribution 4.0 International License. Read Full
License
Page 2/17
Abstract
Introduction: Male sex workers (MSWs) are at high-risk for HIV/STI acquisition. We quantied HIV/STI incidence
rates and identied their time-varying predictors among MSWs in Mexico City.
Methods: MSWs recruited from the largest HIV clinic and community sites in Mexico City were tested for
chlamydia, gonorrhea, syphilis, hepatitis, and HIV at baseline, 6-months, and 12-months. Incidence rates with 95%
bootstrapped condence limits were calculated. We examined potential time-varying predictors using generalized
estimating equations for a population averaged model.
Results and Discussion: Among 227 MSWs, median age was 24 and baseline HIV prevalence was 32%. Incidence
rates (per 100 person-years) were as follows: HIV (5.28; 95%CIs 2.52, 11.07), chlamydia (4.63; 95% 2.41, 8.90),
gonorrhea (3.92; 95% 1.96, 7.84), syphilis (12.44; 95% 8.11, 19.08), hepatitis B (2.09; 95% 0.79, 5.58), hepatitis C
(0.96; 95% 0.24, 3.85), any STI except HIV (17.61; 95% 12.51, 22.72), and any STI including HIV (19.93; 95%CI
14.78, 26.89). In the multivariable-adjusted model, incident STIs (excluding HIV) were lower among those who
reported consistently using condoms during anal and vaginal intercourse (odds ratio (OR) = 0.03, 95% 0.00, 0.68)
compared to those who reported inconsistently using condoms during anal and vaginal intercourse.
Conclusions: HIV/STI incidence is high among MSWs in Mexico City. Consistent condom use is an important
protective factor for HIV/STIs, and should be an important component of interventions to prevent incident
infections.
Introduction
The prevalence of HIV in Mexico is 0.3% in the general adult population, 16.9% among men who have sex with
men, and 18.2% among male sex workers (MSWs) (Galárraga et al., 2014a; Bautista-Arredondo, Colchero, Romero,
Conde-Glez & Sosa-Rubí, 2013). Studies at the global level have shown that, despite a decline in HIV infection in
recent years among the general adult population, HIV acquisition among MSWs has increased (Baral et al., 2015).
In part, this is a result of higher transmissibility of HIV during anal intercourse, as well as other risk factors among
MSWs, including multiple sexual partnerships, membership in dense sexual networks, and limited access to
healthcare services due to stigma (Muraguri et al., 2015; Sethi et al., 2006). Since these factors are predictors of
acquisition of both HIV and other sexually transmitted infections (STIs), it is likely that MSWs in Mexico City are at
an increased risk of all STIs, not just HIV (Finer, Darroch & Singh, 1999; Patra, 2016). However, scant information is
available about the incidence of STIs among MSWs in Mexico City. This is partly due to underreporting of STIs in
Latin American countries, including Mexico, because national STI programs lack consistency about which STIs
they report and how they report them (Garcia, Benzaken, Galban & Members, 2011). Information is also limited
because MSWs are a highly vulnerable and stigmatized population, leading few MSWs to openly disclose their
occupation as sex workers (Closson, Colby, Nguyen, Cohen, Biello & Mimiaga, 2015; WHO, 2013).
Previous studies have quantied STI prevalence in MSW populations; however, no studies have examined STI
incidence rates among MSWs in Mexico City, and this information is essential for health interventions.
Furthermore, no studies have identied predictors of STI acquisition in MSWs in Mexico City or determined how
predictors of STIs vary with time (Vuylsteke et al., 2012; Colby et al., 2015). MSWs are a high-risk population for
HIV/STI acquisition and, due to their behavioral transactions with paying and non-paying male and female
partners, can be at risk for transmitting HIV/STIs to other populations. For example, a recently published modeling
Page 3/17
study (using data from the same study population described below), estimated high rates of HIV transmission
from MSWs to their clients and non-paying partners (approximately 8% per year) (Monteiro et al., 2015). Identifying
predictors of STI incidence is thus essential for developing and targeting interventions to reduce acquisition and
onward transmission within MSW/MSM populations as well as transmission to female populations (Verma &
Collumbien, 2004; Setia, Sivasubramanian, Anand, Row-Kavi & Jerajani, 2010; Hemmige et al., 2011; van Dam &
Holmes, 2000; CDC & World Bank, n.d.). Therefore, our study aims to determine STI/HIV incidence rates, and
identify time-varying predictors of incident STI infection among a sample of MSWs in Mexico City.
Methods
Study Setting and Population
A detailed description of the study population and methods is available elsewhere; a brief overview is provided
here (Galárraga et al., 2014a; Galárraga, Sosa-Rubí, Infante, Gertler & Bertozzi, 2014b). This study is a secondary
analysis of a randomized controlled trial (RCT) that evaluated the impact of conditional economic incentives on
staying free of new curable STIs among MSWs in Mexico City. The RCT was not powered to analyze the effects on
incident STI/HIV by study arm. Thus, we report here the incidence of STI/HIV and its determinants for the entire
sample. This study took place from January 2012 to May 2014. Participants were recruited by trained research
staff from community sites where MSWs were known to congregate in Mexico City, as determined in previous
studies (Galárraga et al., 2014b; Infante, Sosa-Rubí & Caudra, 2009). Participants were also recruited through
referral to the research team from within the Condesa HIV Testing Clinic. Participants were tested and treated for
STIs, as indicated, at
Clínica Condesa
. Treatment was provided free of charge, including antiretroviral treatment for
those identied as HIV-positive. All participants provided informed consent. All procedures were approved by
Institutional Review Boards at Brown University in Providence, USA, and the National Institute of Public Health in
Cuernavaca, Mexico.
The sample consisted of 227 cisgender men, ages 18-40, who either self-identied as MSWs (n=152) or who did
not self-identify as MSW, but who declared that they were a man who had sex with a male partner in exchange for
money in the past six months and who had at least 10 male sexual partners within the last month (n=75). These
criteria were determined based a previous study involving observations and in-depth interviews with sex works in
Mexico City (Infante, Sosa-Rubí & Caudra, 2009). Transgender women were excluded from the present study
because
Clínica Condesa
has a separate program for them.
At the baseline visit, participants lled out a survey with questions regarding sociodemographic characteristics
and health behaviors. At baseline (0 months) and follow-up visits one (6 months) and two (12 months),
participants were tested and treated (as indicated) for syphilis, chlamydia, gonorrhea, and HIV.
Data Collection and Measures
Data collection was done in partnership with the Mexican National Institute of Public Health (INSP) and the
Consortium for HIV/AIDS and TB Research (CISIDAT). Participants were administered the survey using laptop
computers with audio computer assisted interviewing (A-CASI) questionnaires. Blood and urine samples were
obtained from the participants using bio-safety protocols. Samples were analyzed by trained laboratory personnel.
The main outcome of interest was new, conrmed cases of STIs and HIV. Urine specimens were tested for
gonorrhea and chlamydia at the INSP Laboratory (PCR Cobas-Amplicor; Roche, Basel, Switzerland); and blood
Page 4/17
specimens served to measure the presence of HIV, hepatitis B, hepatitis C and syphilis antibodies at the Condesa
Clinic Laboratory (Abbott HIV-1 and HIV-2, Ag/Ab Combo, anti-HBc, anti-HCV and syphilis TP quimioluminiscence
immunoassay (Abbott Laboratories, North Chicago, IL, USA) running in Architect i2000 (Abbott); HIV-positive
samples were conrmed with HIV-1 and HIV-2 CombFirm (Orgenics, Alere, Israel). Anti-HBc+ was tested with
Determine HBsAg and syphilis TP+ (Abbott) with tittered VDRL test (titre ≥ 1:8 was used as the cut-off for active
infection). At the baseline survey, two subgroups were dened for the markers of syphilis and hepatitis B: antibody
positivity was regarded as a lifetime marker of past or present infection, whereas treponemic antibody positivity
together with VDRL demonstrated active syphilis, and anti-HBc plus HBsAg positivity indicated current hepatitis B
virus infection.
Based on ndings from prior literature we created a conceptual framework of likely predictors, the majority of
which were time-varying, and included: age, education, drug use, condom use, and frequency and types of sexual
activities (Patra, 2016; Bazzi et al., 2015). The demographic variable age was continuous and reported in number
of years. The other demographic variable, highest educational attainment, was categorical – it was coded as 1 for
the answer response “Primary or secondary school,” 2 for the answer response “High school,” and 3 for the answer
response “College or higher.” Four separate variables were included to describe sexual activity: had vaginal, anal, or
oral sex with clients last week; had vaginal, anal, or oral sex with romantic partners last week; had insertive anal
sex with any of 3 most recent clients; and had receptive anal sex with any of 3 most recent clients. The rst two
variables describing sexual activity were continuous variables, where respondents reported the number of clients
or romantic partners they had sex with last week. The latter two variables describing sexual activity were also
coded as 0 for the answer response “No” and 1 for the answer response “Yes.” Consistent condom use during sex
in the past month and drug use with any of three most recent clients were similarly coded as 0 for the answer
response “No” and 1 for the answer response “Yes.”
Lastly, since this study is a secondary analysis of a randomized controlled trial (RCT) that evaluated the impact of
conditional economic incentives on staying free of new curable STIs, a variable for randomization to the four
study arms of the original RCT was included in our model. This variable is called conditional economic incentives
and was coded as 1 for no incentive/control, 2 for receiving a Medium incentive to stay free of new curable STIs, 3
for receiving a high incentive to stay free of new curable STIs, and 4 for receiving a medium incentive to attend
study visits only. This controls for the effect of incentives and conditionalities. For further descriptions of the main
covariates and outcomes variables in this study, see Appendix A1.
Income and wealth were not included in the model because nonresponse was high for these variables.
Statistical Analyses
Incidence rates were estimated using the person-time method (i.e., by dividing the total number of new HIV/STI
infections observed during the study period by the total number of person years at risk). We calculated 95%
condence limits using a bias-corrected and accelerated bootstrap method with 1,000 replicates (Efron &
Tibshirani, 1986; Davidson & Hinkley, 1997). We chose this method because it yields appropriate condence
intervals even with relatively small sample sizes. Participants lost to follow-up stopped accruing person years at
their last known study visit. Participants with prevalent HIV infection at baseline were included in the analyses for
incident STIs, but were excluded for analyses estimating HIV incidence. Participants with prevalent STIs at
baseline were excluded for the STIs for which they tested positive, but were still included for calculations of
incident STIs for those which they tested negative at baseline. Since HIV is an incurable STI, someone diagnosed
Page 5/17
with HIV at 6 months would test positive again for HIV at 12 months. Thus, once diagnosed with HIV, individuals
were excluded for analyses estimating HIV incidence but were included in the analyses for other incident STIs.
We estimated marginal models using generalized estimating equations (GEE) with a log link and binomial
variance to examine unadjusted and multivariable-adjusted time-varying predictors of incident STIs (Liang & Zeger,
1986). The GEE model provides marginal estimates, for which the estimate is averaged over all values of the
covariates, which could be correlated. All models used an unstructured correlation structure. In the main analysis,
we used a composite STIs outcome, and then we excluded HIV prevalent cases in a secondary analysis to examine
combined incident STIs/HIV. Data was analyzed using STATA 13.1 (StataCorp LP, College Station, Texas, USA) and
SAS 9.4 (SAS Institute Inc., Cary, North Carolina, USA).
Results
Sociodemographic and behavioral characteristics are shown in Table 1. The median age among MSWs was 24
years, and HIV prevalence at baseline was 32%. The highest level of schooling for 34% of respondents was high
school, while 18% of respondents had attended college or post-graduate school. The majority of MSWs (75%) were
unmarried, yet 43% of MSWs reported having a stable romantic partner. MSWs had a median of three sexual
partners in the last week. About a fth of MSWs (22%) reported being intoxicated while having sex with any of
their three most recent clients, and 22% reported taking drugs before sex with any of their three most recent clients.
The minority of MSWs (29%) reported consistent condom use during sex in the past month. In terms of type of
anal sex, 41% of MSWs had insertive anal sex with any of their three most recent clients, 51% had receptive anal
sex, and 26% had both insertive and receptive anal sex with any of their three most recent clients.
The total amount of follow-up time for the study cohort was 217.25 person-years, and the average follow-up per
participant was 344 days. The highest incidence rates were for active syphilis (12.44 per 100 PY; 95% 8.11, 19.08)
among the entire sample, and HIV (5.28 per 100 PY; 95% 2.52, 11.07) among the HIV-susceptible sample (Table 2).
In the unadjusted GEE models, the odds of incident STIs did not vary signicantly by high school education,
number of clients the individual had sex with in the past week, number of romantic partners the individual had sex
with in the last week, drug use, provision of insertive anal sex, or provision of receptive anal sex (Table 3). The
odds of STIs did differ by age (odds ratio [OR] = 1.45, 95% 1.07, 1.96) and consistent condom use (OR = 0.08, 95%
0.01, 0.90) in the multivariable adjusted model. Sensitivity analyses including incident HIV in a combined HIV/STI
endpoint did not have sucient statistical power (because about a third of the sample was HIV-positive at
baseline and was therefore excluded).
A detailed analysis of loss to follow up for this cohort was conducted in a previous study (Galárraga et al., 2017).
The results of our present GEE model are conditional on returning to the Clinic for follow-up.
Discussion
In this secondary analysis of a randomized controlled trial of MSWs in Mexico City, we found that incidence rates
of HIV/STI were high: incidence of HIV was 5.28 cases/100PY and incidence of syphilis was 12.44 cases/100PY.
In the adjusted multivariable regression models, the only two time-varying predictors found to be signicant was
were age and consistent condom use. Increasing age seems to be a risk factor for incident STIs. Conversely,
consistently using condoms during anal or vaginal intercourse appears to be protective for incident STIs.
Page 6/17
The high HIV and active syphilis incidence rates are consistent with those of other MSW populations in large urban
areas in various places including Kenya, Cote d’Ivoire, Vietnam and the United Kingdom (Muraguri et al., 2015;
Sethi et al., 2006; Vulysteke et al., 2012; Colby et al., 2015). Previous studies of urban, MSM populations have
found a similar correlation between consistent condom use and reduced incident STIs. One study of an HIV
prevention program in southern India found that an increase in consistent condom use by high risk MSM with both
regular male partners (from 33 percent to 46 percent) and paying male partners (from 81 percent to 94 percent)
correlated with a decline in incident syphilis cases in this population (from 14.3 percent to 6.8 percent)
(Subramanian et al., 2013). Another study of MSM in Australia found that, compared to men who reported
consistent condom use during sex, chlamydia incidence was higher among those who reported inconsistent
condom use with either regular sexual partners in the previous 6 months (uHR = 1.3; 95% CI: 0.9–1.8), or with
casual sexual partners in the past 6 months (uHR = 1.6; 95% CI: 1.2–2.1) (Wilkinson et al., 2012). This study also
found that incident chlamydia diagnoses was higher for MSM who self-identied as sex workers (aHR = 1.6; 95%
CI 1.0-2.6). The STI incidence rates from this analysis are also consistent with, although higher than, female sex
worker (FSW) incidence rates found in a study among FSWs in Mexico (Tijuana and Ciudad Juarez): HIV (1.12
cases/100 PY), chlamydia (9.47 cases/100 PY), active syphilis (4.01 cases/100 PY), and gonorrhea (1.78
cases/100 PY) (Strathdee et al., 2013).
It is important to note is that some participants were recruited into our study by referral from within Condesa HIV
Testing Clinic and, furthermore, that participants had to agree to frequent HIV and STI testing as part of the
research protocol. This means study participants likely have a greater concern and interest in their sexual health
than the general MSW population in Mexico City. As such, we expect our estimates for protective health behaviors,
such as condom use, to be overestimates, and we expect estimates for risky health behaviors, such as drug use
during sex work, to be underestimates when compared to the general MSW population in Mexico City. Additionally,
we expect that for some participants recruited from within
Clínica Condesa
the greater concern and interest in their
sexual health, compared to the general MSW population, stems from active STI-like symptoms.
Although our original study did not involve use of PrEP, given the high incidence of HIV within our sample,
availability of and willingness to use PrEP are likely key to shaping effective combination HIV/STI prevention
strategies in the future (Edeza et al. 2020). Previous research in urban centers in Mexico indicates that awareness
and willingness to initiate PrEP is high among MSM (Ravasi et al., 2016; Pitpitan et al., 2015). Yet PrEP is currently
only available in three cities in Mexico and offered to only a limited number of male sex workers and other MSM in
Mexico City. Furthermore, procurement prices continue to be higher in Mexico than other Latin American countries,
which can be a deterrent to larger scale PrEP implementation (Ravasi et al., 2016; Pan American Health
Organization & World Health Organization, 2013). Given the limited availability of PrEP for key populations in
Mexico and the high rate of HIV observed in our sample, it is likely that MSWs in Mexico City would benet from
pre-exposure prophylaxis (PrEP) as part of a combination prevention strategy (Hankins, Macklin & Warren, 2015;
Galea et al., 2011; Liu et al., 1999, Hankins & de Zalduondo, 2010; UNAIDS, 2015).
Since only a small number of MSWs reported consistently using condoms during anal and vaginal sex (28.63%),
interventions that address condom use within this population are crucial for reducing STI risk. The Avahan
Program – a large-scale HIV prevention program in southern India – combines peer-mediated strategies, condom
distribution and STI clinical services to improve outcomes in high-risk men who have sex with men (Subramanian
et al., 2013). Increased condom use with commercial and non-commercial partners, as well as decreased syphilis
incidence, was strongly linked with exposure to this program. In other low and middle income countries, evidence-
Page 7/17
based interventions for increasing condom use in sex worker populations demonstrate that reducing STI
transmission is more effective when combined with the consistent and correct use of condoms (Wariki, Ota, Mori,
Koyanagi, Hori & Shibuya, 2012; Ghys et al., 2001; Laga et al., 1994). This suggests that behavioral interventions
for primary STI and HIV prevention may also serve to enhance the effectiveness of secondary prevention activities.
We also recommend screening MSWs based on self-reported condom use frequency and providing a targeted
HIV/STI prevention and treatment program to those who do not consistently use condoms in order to improve
rates of STI testing, diagnosis, preventative education, and biomedical interventions, such as pre-exposure
prophylaxis (PrEP).
The primary limitation of our study was the calculation of incidence rates using data from a previous randomized
controlled trial of economic incentives to reduce risky sexual practices (Galárraga et al., 2014a). Although the
original pilot intervention was not powered to have a strong and statistically signicant effect on STI/HIV
acquisition compared with the control group, they could have potentially resulted in fewer new STIs cases and
incidence rates that underestimate the true risk in the overall population of MSWs in Mexico City. Therefore, our
results should be interpreted as conservative estimates. Another limitation of the study was the small sample size,
which decreased the precision of our estimates and increased the likelihood of type II error, a failure to detect an
effect that was present within our sample. Some participants were lost-to-follow-up after the rst and second
study appointments, which further reduced the sample size. The smaller sample size, however, did allow us to
collect higher quality data on STIs and potential predictors.
One last element we would like to note is that our nal data collection took place in May 2014. Although there have
inevitably been changes to the eld of HIV and in Mexico City since then, the results of this study are still relevant.
There continues to be a dearth of information on STI and HIV incidence rates among MSWs in Mexico City and in
Latin American more generally. To the best of our knowledge, this is the only study that provides these incidence
rates for MSWs in Mexico City. Furthermore, prevention and early detection of HIV are both as important as ever.
Our model is key in illuminating modiable risk factors for prevention of STI and HIV acquisition.
Conclusions
This study found that MSWs in Mexico City have a high incidence of STIs, particularly HIV and active syphilis.
Consistently using condoms during anal and vaginal sex was found to be associated with a lower likelihood of STI
acquisition among these MSWs. Consistent condom use appears to be a key potential predictor of STIs and is an
important component of interventions to prevent infections. Additionally, targeted interventions for MSWs who
report inconsistent condom use are warranted in light of these ndings. Given such high HIV rates within this MSW
population, the population would likely benet from future work that assesses the feasibility, effects, and cost of
incorporating PrEP in multidimensional interventions.
Abbreviations
Not applicable.
Declarations
Ethics Approval and Consent to Participate
Page 8/17
All participants in this study provided informed consent. All procedures were approved by Institutional Review
Boards at Brown University in Providence, USA, and the National Institute of Public Health in Cuernavaca, Mexico.
Consent for Publication
Not applicable.
Availability of Data and Materials
Study data is available from the authors upon request.
Funding
Funding: US National Institutes of Health (R21-HD065525 “Conditional economic incentives to reduce HIV risk: A
pilot in Mexico” and R34-MH114664 “ PrEP Seguro: Antiretrovial-Based HIV Prevention Among Men at High Risk in
Mexico”; PI: Galárraga). Additional support was provided to A. Zullo by the Agency for Healthcare Research and
Quality (K12-HS022998). B. Marshall is supported by the National Institute on Drug Abuse (DP2-DA040236) and
by a Henry Merrit Wriston Fellowship from Brown University; and M. Lurie is supported in part by US NIH National
Institute of Child Health and Development grant (R24-HD077976) and 1R01 MH106600-01 from the National
Institute of Mental Health.
This research also beneted from support to the Population Studies and Training Center (PSTC) at Brown
University, which receives core support from the Eunice Kennedy Shriver National Institute of Child Health and
Human Development (P2C-HD041020). The views and opinions expressed are those of the authors alone and do
not necessarily represent those of Brown University, the Corporation or Trustees. The funding organizations did not
have any role in the decisions to conduct the trial, analyze data, or prepare manuscripts for publication.
Competing Interests
The authors declare they have no competing interests.
Authors’ Contributions
OG, SGSR, and DO conducted the original study that produced the dataset for the current study. OG conceived of
the initial idea for this study, which was subsequently rened by the other authors. KYG, MW, and ARZ conducted
the data analysis and wrote the initial draft of the manuscript. All authors provided input on the interpretation of
the results, revising the work for important intellectual content, approved the nal version of the work, and agree to
be accountable for all aspects of the work.
Acknowledgements
We gratefully acknowledge the Clínica Condesa staff members; particularly Andrea González, Florentino Badial,
Nathalie Gras, and Jehovani Tena; as well as Luis Juarez and his staff at the Clínica Condesa Laboratory, which
conducted most of the biological testing. We also acknowledge the following Mexican National Institute of Public
Health (INSP) staff: Biani Saavedra, and María Olmendi. The INSP STI Laboratory processed testing for Chlamydia
and Gonorrhea. Database construction by CEO: Edgar Díaz. Project management and administration by CISIDAT
(Consortium for HIV/AIDS and TB Research). We especially thank the participants for agreeing to become part of
Punto Seguro
.
Page 9/17
References
Baral, S. D., Friedman, M. R., Geibel, S., Rebe, K., Bozhinov, B., Diouf, D., … Cáceres, C. F. (2015). Male sex workers:
practices, contexts, and vulnerabilities for HIV acquisition and transmission.
The Lancet
,
385
(9964), 260–273.
https://doi.org/10.1016/S0140-6736(14)60801-1
Bautista-Arredondo, S., Colchero, M. A., Romero, M., Conde-Glez, C. J., & Sosa-Rubí, S. G. (2013). Is the HIV
Epidemic Stable among MSM in Mexico? HIV Prevalence and Risk Behavior Results from a Nationally
Representative Survey among Men Who Have Sex with Men.
PLOS ONE
,
8
(9), e72616.
https://doi.org/10.1371/journal.pone.0072616
Bazzi, A. R., Rangel, G., Martinez, G., Ulibarri, M. D., Syvertsen, J. L., Bazzi, S. A., … Strathdee, S. A. (2015). Incidence
and Predictors of HIV and Sexually Transmitted Infections Among Female Sex Workers and Their Intimate Male
Partners in Northern Mexico: A Longitudinal, Multilevel Study.
American Journal of Epidemiology
,
181
(9), 723–
731. https://doi.org/10.1093/aje/kwu340
CDC, World Bank. (n.d.).
Sexually Transmitted Infections in Developing Countries: Current concepts and strategies
on improving STI prevention, treatment, and control
(p. 55).
Closson, E. F., Colby, D. J., Nguyen, T., Cohen, S. S., Biello, K., & Mimiaga, M. J. (2015). The balancing act: Exploring
stigma, economic need and disclosure among male sex workers in Ho Chi Minh City, Vietnam.
Global Public
Health
,
10
(4), 520–531. https://doi.org/10.1080/17441692.2014.992452
Colby, D. J., Oldenburg, C. E., Nguyen, T., Closson, E. F., Biello, K. B., Mayer, K. H., & Mimiaga, M. J. (2015). HIV,
Hepatitis C, and Other Sexually Transmitted Infections Among Male Sex Workers in Ho Chi Minh City, Vietnam.
AIDS and Behavior
,
20
(4), 768–775. https://doi.org/10.1007/s10461-015-1247-z
Davison, A. C., & Hinkley, D. V. (1997).
Bootstrap methods and their application
.
https://doi.org/10.1017/CBO9780511802843
Edeza, A., Galárraga, O., Santamaria, E. K., Sosa-Rubí, S., Operario, D., & Biello, K. B. (2020). “I Do Try To Use
Condoms, But…”: Knowledge and Interest in PrEP Among Male Sex Workers in Mexico City.
Archives of Sexual
Behavior
,
49
(1), 355–363. https://doi.org/10.1007/s10508-019-01473-4
Efron, B., & Tibshirani, R. (1986). Bootstrap Methods for Standard Errors, Condence Intervals, and Other Measures
of Statistical Accuracy.
Statistical Science
,
1
(1), 54–75. https://doi.org/10.1214/ss/1177013815
Finer, L. B., Darroch, J. E., & Singh, S. (1999). Sexual partnership patterns as a behavioral risk factor for sexually
transmitted diseases.
Family Planning Perspectives
,
31
(5), 228–236.
Galárraga, O., Sosa-Rubí, S. G., Kuo, C., Gozalo, P., González, A., Saavedra, B., Gras-Allain, N., Conde-Glez, C. J.,
Olamendi-Portugal, M., Mayer, K. H., & Operario, D. (2017). Punto Seguro: A Randomized Controlled Pilot Using
Conditional Economic Incentives to Reduce Sexually Transmitted Infection Risks in Mexico.
AIDS and Behavior
,
21
(12), 3440–3456. https://doi.org/10.1007/s10461-017-1960-x
Galárraga, O., Sosa-Rubí, S. G., González, A., Badial-Hernández, F., Conde-Glez, C. J., Juárez-Figueroa, L., … Mayer, K.
H. (2014). The disproportionate burden of HIV and STIs among male sex workers in Mexico City and the rationale
Page 10/17
for economic incentives to reduce risks.
Journal of the International AIDS Society
,
17
(1).
https://doi.org/10.7448/IAS.17.1.19218
Galárraga, O., Sosa-Rubí, S. G., Infante, C., Gertler, P. J., & Bertozzi, S. M. (2014). Willingness-to-accept reductions in
HIV risks: conditional economic incentives in Mexico.
The European Journal of Health Economics: HEPAC: Health
Economics in Prevention and Care
,
15
(1), 41–55. https://doi.org/10.1007/s10198-012-0447-y
Galea, J. T., Kinsler, J. J., Salazar, X., Lee, S.-J., Giron, M., Sayles, J. N., … Cunningham, W. E. (2011). Acceptability of
Pre-Exposure Prophylaxis (PrEP) as an HIV prevention strategy: Barriers and facilitators to PrEP uptake among at-
risk Peruvian populations.
International Journal of STD & AIDS
,
22
(5), 256–262.
https://doi.org/10.1258/ijsa.2009.009255
Garcia, P. J., Benzaken, A. S., Galban, E., & Members, the A.-I. (2011). STI management and control in Latin
America: where do we stand and where do we go from here?
Sexually Transmitted Infections
,
87
(Suppl 2), ii7-ii9.
https://doi.org/10.1136/sextrans-2011-050177
Ghys, P. D., Diallo, M. O., Ettiègne-Traoré, V., Satten, G. A., Anoma, C. K., Maurice, C., … Laga, M. (2001). Effect of
interventions to control sexually transmitted disease on the incidence of HIV infection in female sex workers.
AIDS
(London, England)
,
15
(11), 1421–1431.
Hankins, C. A., & de Zalduondo, B. O. (2010). Combination prevention: a deeper understanding of effective HIV
prevention:
AIDS
,
24
(Suppl 4), S70–S80. https://doi.org/10.1097/01.aids.0000390709.04255.fd
Hankins, C., Macklin, R., & Warren, M. (2015). Translating PrEP effectiveness into public health impact: key
considerations for decision-makers on cost-effectiveness, price, regulatory issues, distributive justice and
advocacy for access.
Journal of the International AIDS Society
,
18
(4Suppl 3).
https://doi.org/10.7448/IAS.18.4.19973
Hemmige, V., Snyder, H., Liao, C., Mayer, K., Lakshmi, V., Gandham, S. R., … Schneider, J. (2011). Sex position,
marital status, and HIV risk among Indian men who have sex with men: clues to optimizing prevention
approaches.
AIDS Patient Care and STDs
,
25
(12), 725–734. https://doi.org/10.1089/apc.2011.0079
Infante, C., Sosa-Rubi, S. G., & Cuadra, S. M. (2009). Sex work in Mexico: vulnerability of male, travesti, transgender
and transsexual sex workers.
Culture, Health & Sexuality
,
11
(2), 125–137.
https://doi.org/10.1080/13691050802431314
Laga, M., Alary, M., Behets, F., Goeman, J., Piot, P., Nzila, N., … St Louis, M. (1994). Condom promotion, sexually
transmitted diseases treatment, and declining incidence of HIV-1 infection in female Zairian sex workers.
The
Lancet
,
344
(8917), 246–248. https://doi.org/10.1016/S0140-6736(94)93005-8
Liang, K.-Y., & Zeger, S. L. (1986). Longitudinal data analysis using generalized linear models.
Biometrika
,
73
(1),
13–22. https://doi.org/10.1093/biomet/73.1.13
Liu, A. Y., Kittredge, P. V., Vittinghoff, E., Raymond, H. F., Ahrens, K., Matheson, T., … Buchbinder, S. P. (2008). Limited
knowledge and use of HIV post- and pre-exposure prophylaxis among gay and bisexual men.
Journal of Acquired
Immune Deciency Syndromes (1999)
,
47
(2), 241–247.
Page 11/17
Monteiro, J. F. G., Marshall, B. D. L., Escudero, D., Sosa-Rubí, S. G., González, A., Flanigan, T., … Galárraga, O. (2015).
Preventing HIV Transmission Among Partners of HIV-Positive Male Sex Workers in Mexico City: A Modeling Study.
AIDS and Behavior
,
19
(9), 1579–1588. https://doi.org/10.1007/s10461-014-0915-8
Muraguri, N., Tun, W., Okal, J., Broz, D., Raymond, H. F., Kellogg, T., … Geibel, S. (2015). HIV and STI Prevalence and
Risk Factors Among Male Sex Workers and Other Men Who Have Sex With Men in Nairobi, Kenya:
JAIDS Journal
of Acquired Immune Deciency Syndromes
,
68
(1), 91–96. https://doi.org/10.1097/QAI.0000000000000368
Pan American Health Organization, & World Health Organization. (2013).
Antiretroviral treatment in the spotlight: a
public health analysis in Latin America and the Caribbean, 2013
. Retrieved from
http://iris.paho.org/xmlui/handle/123456789/31367?locale-attribute=pt
Patra, S. (2016). Socio-cultural correlates and risky sexual behaviour inuencing prevalence of HIV/AIDS and STIs
in Uganda: A gender perspective.
Cogent Social Sciences
,
2
(1), 1166472.
https://doi.org/10.1080/23311886.2016.1166472
Pitpitan, E. V., Goodman-Meza, D., Burgos, J. L., Abramovitz, D., Chavarin, C. V., Torres, K., … Patterson, T. L. (2015).
Prevalence and correlates of HIV among men who have sex with men in Tijuana, Mexico.
Journal of the
International AIDS Society
,
18
, 19304. https://doi.org/10.7448/IAS.18.1.19304
Ravasi, G., Grinsztejn, B., Baruch, R., Guanira, J. V., Luque, R., Cáceres, C. F., & Ghidinelli, M. (2016). Towards a fair
consideration of PrEP as part of combination HIV prevention in Latin America.
Journal of the International AIDS
Society
,
19
(7 (Suppl 6)). https://doi.org/10.7448/IAS.19.7.21113
Sethi, G., Holden, B. M., Gaffney, J., Greene, L., Ghani, A. C., & Ward, H. (2006). HIV, sexually transmitted infections,
and risk behaviours in male sex workers in London over a 10 year period.
Sexually Transmitted Infections
,
82
(5),
359–363. https://doi.org/10.1136/sti.2005.019257
Setia, M. S., Sivasubramanian, M., Anand, V., Row-Kavi, A., & Jerajani, H. R. (2010). Married men who have sex with
men: the bridge to HIV prevention in Mumbai, India.
International Journal of Public Health
,
55
(6), 687–691.
https://doi.org/10.1007/s00038-010-0173-0
Strathdee, S. A., Abramovitz, D., Lozada, R., Martinez, G., Rangel, M. G., Vera, A., … Patterson, T. L. (2013).
Reductions in HIV/STI incidence and sharing of injection equipment among female sex workers who inject drugs:
results from a randomized controlled trial.
PloS One
,
8
(6), e65812. https://doi.org/10.1371/journal.pone.0065812
Subramanian, T., Ramakrishnan, L., Aridoss, S., Goswami, P., Kanguswami, B., Shajan, M., … Paranjape, R. S.
(2013). Increasing condom use and declining STI prevalence in high-risk MSM and TGs: evaluation of a large-
scale prevention program in Tamil Nadu, India.
BMC Public Health
,
13
(1). https://doi.org/10.1186/1471-2458-13-
857
UNAIDS. (2015).
Fast-Tracking combination prevention: Towards Reducing New HIV Infections to Fewer Than 500
000 by 2020
. Retrieved from
http://www.unaids.org/en/resources/documents/2015/20151019_JC2766_Fast_tracking_combination_prevention
van Dam, C. J., & Holmes, K. K. (2000). STD prevention: effectively reaching the core and a bridge population with
a four-component intervention.
Sexually Transmitted Diseases
,
27
(1), 9–11.
Page 12/17
Verma, R. K., & Collumbien, M. (2004). Homosexual activity among rural Indian men: implications for HIV
interventions.
AIDS (London, England)
,
18
(13), 1845–1847.
Vuylsteke, B., Semde, G., Sika, L., Crucitti, T., Ettiegne Traore, V., Buve, A., & Laga, M. (2012). High prevalence of HIV
and sexually transmitted infections among male sex workers in Abidjan, Côte d’Ivoire: need for services tailored to
their needs.
Sexually Transmitted Infections
,
88
(4), 288–293. https://doi.org/10.1136/sextrans-2011-050276
Wariki, W. M., Ota, E., Mori, R., Koyanagi, A., Hori, N., & Shibuya, K. (2012). Behavioral interventions to reduce the
transmission of HIV infection among sex workers and their clients in low- and middle-income countries.
Cochrane
Database of Systematic Reviews
. https://doi.org/10.1002/14651858.CD005272.pub3
WHO | Implementing comprehensive HIV/STI programmes with sex workers: practical approaches from
collaborative interventions. (2013). Retrieved May 10, 2016, from WHO website:
http://www.who.int/hiv/pub/sti/sex_worker_implementation/en/
Wilkinson, A., El-Hayek, C., Fairley, C. K., Leslie, D., Roth, N., Tee, B. K., … Stoové, M. (2012). Incidence and risk
factors associated with chlamydia in men who have sex with men: a cohort analysis of Victorian Primary Care
Network for Sentinel Surveillance data.
Sexually Transmitted Infections
,
88
(5), 319–324.
https://doi.org/10.1136/sextrans-2011-050270
Tables
Table 1. Baseline Characteristics of Male Sex Workers (N=227) in Mexico City
Page 13/17
Characteristic n (%)
Demographics
Age, years 24 (20-27), Median (IQR)
Highest educational attainment
Primary or secondary school 92 (40.53)
High school 77 (33.92)
College or post-graduate 41 (18.06)
Marital status
Single 171 (75.33)
Married/free union 42 (18.50)
Divorced/separated 2 (0.88)
Stable romantic partner 97 (42.73)
Sexual Behaviors
Number of male clients in the past week 4.55 (4.98), % Mean (SD)
Number of female clients in the past week 2.53 (6.03) % Mean (SD)
Number of people individual had vaginal
or anal or oral sex with last week
3 (1-6), Median (IQR)
Intoxicated while having sex with any of
three most recent clients
49 (21.59)
Used drugs before having sex with any
of three most recent clients
49 (21.59)
Consistently used condoms during sex
in past month
65 (28.63)
Had insertive anal sex with any of
three most recent clients
94 (41.41)
Had receptive anal sex with any of
three most recent clients
116 (51.10)
Had receptive and insertive anal sex
with any of three most recent clients
58 (25.55)
Table 1. (Continued)
Page 14/17
Characteristic n (%)
STI Prevalence
Positive STI test result
HIV 73 (32.16)
Chlamydia 23 (10.13)
Gonorrhea 4 (1.76)
Active syphilis 42 (18.50)
Hepatitis B 20 (8.81)
Hepatitis C 2 (0.88)
Any STI (except HIV) 76 (33.48)
Any STI (including HIV) 116 (51.10)
Notes: Table shows number of cases and percentage in parentheses unless otherwise noted.
N = total respondents; IQR = interquartile range, SD = standard deviation
Table 2. Incidence of HIV and STIs among Male Sex Workers in Mexico City
STI New Cases Rate (Cases/100 PY [95%CI]1)
HIV 7 5.28 (2.52, 11.07)
Chlamydia 9 4.63 (2.41, 8.90)
Gonorrhea 8 3.92 (1.96, 7.84)
Active Syphilis 21 12.44 (8.11, 19.08)
Hepatitis B 4 2.09 (0.79, 5.58)
Hepatitis C 2 0.96 (0.24, 3.85)
Any STI (except HIV) 44 17.61 (12.51, 22.72)
Any STI (including HIV) 51 19.93 (14.78, 26.89)
Abbreviations: STI, sexually transmitted infection; PY, person-years; CI, condence intervals.
1Calculated using person-clustered, bias-corrected, accelerated bootstrapping with 1000 replications.
New Cases = instances of new cases during study
Table 3. Associations between Predictors and Incident STIs*
Page 15/17
Characteristic Unadjusted
OR (95%CI)
Adjusted
OR (95%CI)
Demographics
Age, years 1.02 (0.95,
1.09) 1.45 (1.07, 1.96)
Highest educational attainment
Primary or secondary school ref ref
High school 1.30 (0.62,
2.70) 1.23 (0.13,
11.42)
College or post-graduate 0.75 (0.29,
1.94) 0.43 (0.02, 9.97)
Sexual Behaviors
Had vaginal, anal, or oral sex with clients last week, number of
clients 0.98 (0.87,
1.10) 1.35 (0.70, 2.61)
Had vaginal, anal, or oral sex with people last week, number of
people 0.99 (0.94,
1.03) 0.74 (0.38, 1.42)
Used drugs while having sex with any of
three most recent clients
0.33 (0.09,
1.15) 2.07 (0.18,
23.46)
Consistently used condoms during sex in past month 0.76 (0.38,
1.50) 0.03 (0.00, 0.68)
Had insertive anal sex with any of
3 most recent clients
0.65 (0.25,
1.71) 3.26 (0.44,
24.32)
Had receptive anal sex with any of
3 most recent clients
2.05 (0.75,
5.64) 2.78 (0.27,
28.34)
Conditional Economic Incentives
Control/No incentive ref ref
Medium incentive for staying free of STIs 2.24 (0.80,
6.30) 0.45 (0.02,
11.93)
High incentive for staying free of STIs 2.89 (1.04,
8.01) 0.05 (0.00, 2.24)
Medium incentive for study visits only 2.32 (0.84,
6.45) 0.04 (0.00, 1.90)
Notes: Abbreviations: STI, sexually transmitted infections; OR, odds ratio; ref, reference level.
*Prevalent cases of HIV were retained in the analyses as still susceptible for other STIs. Prevalent cases of STI
were retained in analyses as still susceptible for STIs for which they tested negative.
Appendix
Page 16/17
Appendix A1. Description of Main Covariates and Outcome Variables
Variable Question Answer Options Coding for the
Analysis
Demographics
Age How old are you? Discrete variable; 99.I don’t want to answer Discrete variable
Highest
educational
attainment
What is the highest
level of education
you have
completed?
0.Didn’t complete primary; 1.Primary;
2.Secondary; 3.High School; 4.College; 5.Graduate
School; 99.I don’t wish to answer
1.Primary or
secondary
school; 2.High
school; 3.College
or higher
Sexual Behaviors
Had
vaginal,
anal, or oral
sex with
clients last
week
With how many
clients did you have
vaginal or anal or
oral sex with during
the last week?
Number of male clients (discrete variable);
Number of female clients (discrete variable); 888.I
don’t know; 999. I don’t wish to answer
Total number of
clients (discrete
variable)
Had
vaginal,
anal, or oral
sex with
people last
week
With how many
romantic partners
did you have vaginal
or anal or oral sex
with during the last
week?
Number of male romantic partners (discrete
variable); Number of female romantic partners
(discrete variable); 888.I don’t know; 999. I don’t
wish to answer
Total number of
romantic
partners
(discrete
variable)
Used drugs
while
having sex
with any of
3 most
recent
clients
Before being with
your last client, did
you take any drugs?
†
1.Yes; 3.No; 99.I don’t wish to answer 0.No; 1.Yes (used
drugs before
having sex with
at least one of 3
most recent
clients)
Consistently
used
condoms
during sex
in past
month
When you had sex,
how often did you
use condoms in the
past month?
0.Never; 1.Almost never; 2.Sometimes; 3.Almost
every time; 4.Every time 0.Almost every
time, sometimes,
almost never, or
never; 1.Every
time
Had
insertive
anal sex
with any of
3 most
recent
clients
Did you provide the
services that your
most recent client
requested? If yes,
how many times?†
Discrete variables: 1.Talk, 2.Insertive anal sex (he
penetrated you), 3.Receptive anal sex (you
penetrated him), 4.Oral sex, 5.Masturbating,
6.Dance, 7.Bathing, 8.Massage, 9.Striptease,
10.Vaginal sex. 99.Do not wish to answer
0.No; 1.Yes (had
insertive anal
sex with at least
one of 3 most
recent clients)
Appendix A1. (Continued)
Page 17/17
Variable Question Answer Options Coding for
the Analysis
Sexual Behaviors (continued)
Had
receptive
anal sex
with any of
3 most
recent
clients
Did you provide the
services that your
most recent client
requested? If yes,
how many times?†
Discrete variables: 1.Talk, 2.Insertive anal sex (he
penetrated you), 3.Receptive anal sex (you penetrated
him), 4.Oral sex, 5.Masturbating, 6.Dance, 7.Bathing,
8.Massage, 9.Striptease, 10.Vaginal sex. 99.Do not
wish to answer
0.No; 1.Yes
(had
receptive
anal sex
with at least
one of 3
most recent
clients)
STI Incidence
New
sexually
transmitted
infections
(STIs) and
HIV
Participants provided blood and urine samples, collected following the local
biosafety protocols by trained staff and analyzed by lab technicians. Urine
specimens were tested for gonorrhea and chlamydia (PCR Cobas-Amplicor;
Roche, Basel, Switzerland); blood specimens served to measure presence of HIV,
hepatitis B, hepatitis C and syphilis antibodies (Abbott HIV-1 and HIV-2, Ag/Ab
Combo, anti-HBc, anti-HCV and syphilis TP quimioluminiscence immunoassay;
Abbott Laboratories, North Chicago, IL, USA) running in Architect i2000 (Abbott).
HIV+ samples were conrmed with HIV-1 and HIV-2 CombFirm (Orgenics, Yavne,
Israel); and anti-HBcwas tested with Determine HBsAg and syphilis TP (Abbott)
with tittered VDRL, the Venereal Disease Research Laboratory test. Two
subgroups were dened for the markers of Syphilis: antibody positivity was
regarded as a lifetime marker of past or present infection, whereas treponemic
antibody positivity together with VDRL demonstrated active syphilis.
0.No 1.Yes
(any new
STI/HIV)
Randomization
Conditional
Economic
Incentives
Participants were randomizedand allocated into one of four groups: control,
medium incentive to stay free of new curable STIs (USD $50), high incentive to
stay free of new curable STIs (USD $75), or medium incentive to attend study
visits (USD $50).§
1.Control/no
incentive;
2.Medium
incentive to
stay free of
new curable
STIs; 3.High
incentive to
stay free of
new curable
STIs;
4.Medium
incentive to
attend study
visits
Notes: †The same question was asked about next-to-last client and second-to-last client; §Approximate average
exchange rate at time of study (2012–14): 12 Mexican Pesos per $1 (USD).