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Original article
Syphilis infection, sexual practices and bisexual behaviour among men who have sex with men and transgender women: a cross-sectional study
  1. Fernanda Rodas Pires Fernandes1,
  2. Priscila Brunini Zanini1,
  3. Grazielli Rocha Rezende1,
  4. Lisie Souza Castro1,
  5. Larissa Melo Bandeira1,
  6. Marco Antônio Puga1,
  7. Tayana Serpa Ortiz Tanaka1,
  8. Ludiele Souza Castro1,
  9. Lívia Garcia Bertolacci-Rocha1,
  10. Sheila Araújo Teles2,
  11. Ana Rita Coimbra Motta-Castro1,3
  1. 1Laboratory of Clinical Immunology, Federal University of Mato Grosso do Sul, Campo Grande, MS, Brazil
  2. 2School of Nursing, Federal University of Goias, Goiânia, GO, Brazil
  3. 3Laboratory of Molecular Virology, Oswaldo Cruz Foundation, Mato Grosso do Sul, Brazil
  1. Correspondence to Fernanda Rodas Pires Fernandes, Federal University of Mato Grosso do Sul, Caixa Postal 549, Campo Grande, MS CEP 79070900, Brazil; ferodas{at}hotmail.com

Abstract

Objectives Men who have sex with men (MSM) and transgender women (TW) are highly vulnerable groups to sexually transmitted infections (STIs). This study aims to assess the prevalence of syphilis infection, sexual behaviour and identify factors associated with syphilis in MSM and TW in Campo Grande, Central Brazil.

Methods Between 2009 and 2011, 430 MSM/TW participants were interviewed and tested for syphilis. Univariable and multivariable regression analyses were done to assess associations with syphilis infection.

Results A total of 430 MSM/TW (278 MSM and 152 TW) were included in the study. The overall prevalence of lifetime syphilis and active syphilis was 34.7% (26.3% among MSM; 50.0% among TW) and 17.5% (12.3% among MSM; 27.0% among TW), respectively (p<0.001). In multivariable regression analysis, being 20–24 years and ≥30 years, having engaged in a variety of sexual practices and with a history of genital/anal ulcer in the last 12 months were associated with lifetime syphilis infection in the MSM group. Among TW participants, being ≥30 years of age, having more than 10 male sexual partners in last week and being infected with HIV were associated with lifetime syphilis. Factors associated with active syphilis among MSM were massage parlour/sauna recruitment and alcohol consumption at least once a week. Having sex with female partners in the past 12 months was predictive for active syphilis among TW.

Conclusions The prevalence of syphilis infection and risk sexual behaviour were high in the two samples, especially among TW. High levels of bisexual behaviours and low rates of consistent condom use indicate potential HIV/STIs transmission into the heterosexual population. This finding indicates the need and urgency for implementing more effective integrated programmes targeting MSM/TW for the prevention of syphilis and other STIs.

  • SYPHILIS
  • TRANSSEXUAL
  • SEXUAL BEHAVIOUR
  • MEN
  • EPIDEMIOLOGY (GENERAL)
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Introduction

Syphilis is an ulcerative sexually transmitted infection (STI) caused by the spirochaete Treponema pallidum subspecies pallidum. The infection is systemic, usually involving cutaneous manifestations in early stage, with a range of serious complications including cardiovascular and neurological disease in later stage.1 Syphilis infection remains an alarming public health problem worldwide with an estimated 36 million prevalent cases globally and over 11 million incident cases annually.2

Despite inexpensive and effective antibiotic therapy, syphilis has increased significantly among young adults and sexual intercourse has been reported as the main transmission route.3 ,4 Men who have sex with men (MSM) and transgender women (TW) are highly vulnerable to STIs because of high levels of unprotected sexual practices and multiple sexual partners.5 ,6 Social stigmatisation and homophobia contribute to low self-esteem, isolation and depression. These are all known correlates of unintended high-risk behaviours, common psychological disorders and substance abuse. In addition, studies suggest that a large proportion of TW engage in commercial sex work attributable, in part, to social exclusion and the lack of employment opportunities due to transgender discrimination.7 ,8

Recently, interest in syphilis has grown because the presence of ulcerative lesions has been shown to be a risk factor of acquisition and transmission of HIV.9 MSM/TW play a bridging role in the transmission of HIV and other STIs to sexual networks in which the majority is heterosexual.10 ,11 Several studies have shown significantly higher rates of sexual risk behaviours and syphilis infection among MSM.12–14

In order to implement appropriate prevention measures, it is important to understand the risk sexual factors for syphilis infection among MSM and TW. MSM and TW studies in Brazil are limited, given the difficulties in accessing this stigmatised hidden population. This is the first study on socio-demographic characteristics, sexual practices, drug use behaviours and the prevalence of syphilis among MSM and TW in the Midwestern region of Brazil.

Material and methods

This cross-sectional study was conducted among MSM/TW in Campo Grande city, Brazil, from November 2011 to September 2013. The study participants were divided into two groups, MSM and TW, according to the self-designation of the individuals during the interview. TW was defined as a group of individuals who were born male but who are identified as a different gender. In Brazil, they include crossdressers or transvestites (those who desire to wear clothing associated with another sex) and male-to-female transexuals (those who desire or have undergone sexual reassignment surgery or altered their bodies with hormone therapy and silicone injections). MSM and TW were previously contacted through the Mato Grosso do Sul State Association of Travestites and Transsexuals and Reference Center for Human Rights in the Prevention and Combat of Homophobia. Participants were also recruited from public (e.g., bars, parks, streets) and private (e.g., massage parlours, saunas, nightclubs) places frequented by them. Subjects were eligible to participate if they were male sex, older than 18 years, self-reported having sex with other men in the past 12 months and were able to provide written informed consent. After providing informed consent, all participants were interviewed face-to-face by trained health professionals using a standardised questionnaire with information regarding socio-demographic characteristics and sexual behaviour. Along with counselling, printed and oral information on HIV and STI prevention was given. Blood samples were collected for syphilis and HIV screening.

The lifetime syphilis infection was determined using an enzyme immunoassay (EIA) (ICE Syphilis, DiaSorin, UK). EIA-reactive samples were serially diluted to quantify Venereal Disease Research Laboratory (VDRL) titres, with active syphilis defined as a VDRL ≥1:16. HIV infection was identified by screening with EIA and confirmation by western blot assay (Novopath HIV-I, Immunoblot, BioRad).

Questionnaire-based data and biological testing results were recorded, double checked and entered into EPI-INFO 3.4.1 (Center for Diseases Control and Prevention, Atlanta, Georgia, USA, 1997) statistical software package. Due to the high prevalence of syphilis infection among MSM/TW, prevalence ratios were used to estimate the level of association between lifetime syphilis infection and potential risk factors. Poisson regression models were used for data analysis (STATA V.13.1 for Windows). The study was approved by the Committee for Human Research of the Federal University of Mato Grosso do Sul.

Results

Socio-demographic and behavioural characteristics

Of the 535 men invited to participate, 430 (80.4%) agreed to the interview and also provided biological samples. The study included 278 MSM and 152 TW. Socio-demographic characteristics, sexual behaviours and substance use of the study sample are presented in table 1, separately for MSM and TW. Differences between TW and MSM groups were noted for almost all variables, highlighting the importance of analysing these groups separately. MSM group had a median age of 25 years (from 18 to 61 years), while TW had a median age of 27 years (from 18 to 70 years). Both groups (91.4% of MSM and 80.3% of TW) were predominantly unmarried (single, divorced or widowed) and 12.6% of all participants reported as being married to MSM or women.

Table 1

Socio-demographic characteristics, substance use and sexual risks among men who have sex with men (MSM) and transgender women (TW)

Recreational drug use differed substantially by group (p<0.001). Concomitant use of inhaled cocaine and marijuana smoking were frequently reported (95.7%) among drug using participants, followed by cocaine paste (intermediary product of the cocaine preparation process) (11.4%), crack (6.7%), ecstasy (4.3%) and other drugs (6.2%). Exchange of sex for money or goods was reported by 37% of the participants overall, and was more common among TW than MSM (p<0.001). Of these, 32.1% reported irregular condom use for anal sex with clients in the last month and 6.3% related non-condom use in the last anal intercourse. Unprotected oral intercourse with clients in the last contact sexual was reported by 28.9% of sex workers. A higher percentage of TW reported elevated number of male sexual partners in the last week, non-condom use with the sexual partners in the last year, experiencing sexual coercion and a history of ever having engaged in a variety of practices. The prevalence of diverse sexual practices was as follows: rimming (53.6%), sadism and/or masochism (35.9%), water sports (28.1%), group sex (10.5%) and others (20.3%) (fisting, shared sex toys and others).

Syphilis infection and associated risk factors

The prevalence of lifetime syphilis (any VDRL titre) among MSM/TW was 34.7% (149/430; 95% CI 30.2 to 39.1): 26.3% (95% CI 21.1 to 31.4) among MSM and 50.0% (95% CI 42.1 to 57.9) among TW (p<0.001). Prevalence of active syphilis was 17.5% among MSM/TW (75/430; 95% CI 13.9 to 21.0). Among MSM, this rate was 12.3% (34/278; 95% CI 8.4 to 16.1) and 27.0% among TW (41/152; 95% CI 8.4 to 16.1) (p<0.001). Table 2 presents the univariable regression analysis of variables associated with syphilis infection among MSM and TW. In multivariable analysis (table 3), aged 20–24 years and over 29 years old, diverse sexual practices and history of genital/anal ulcer in the last 12 months were associated with lifetime syphilis in the MSM group. Among TW participants, older age, having had more than 10 male sexual partners in last week and HIV infection were associated with lifetime syphilis. Factors associated with active syphilis among MSM were massage parlour/sauna recruitment and alcohol consumption at least once a week. Among TW, having sex with female partners in the past 12 months was predictive of active infection.

Table 2

Univariable regression analysis of risk factors associated with syphilis prevalence among men who have sex with men (MSM) and transgender women (TW)

Table 3

Multivariable regression analysis of risk factors associated with syphilis infection among men who have sex with men (MSM) and transgender women (TW)

After controlling for significant variables identified on univariable analysis, having sex with female partners in the past 12 months was a protective factor against active syphilis among MSM.

Discussion

The present study found high levels of syphilis infection and substantial differences for risky sexual behaviours between MSM and TW groups from Central Brazil. The prevalence of active syphilis in these groups of MSM and TW was notably higher than other studies conducted among MSM/TW from other countries and in Brazil.15–21 The prevalence of syphilis infection detected in TW was alarmingly higher than that found among MSM, likely reflecting the higher number of sexual partners, low condom use rates, illicit drugs use, history of sexual coercion and low educational level reported by them. This result is consistent with the studies reported by Pisani et al15 and Farías et al.13 These high rates of active syphilis are not only established indicators of risky sexual behaviours but are associated with sexual transmission of HIV due to the presence of genital ulceration.9 In this scenario, intervention efforts for controlling the epidemics of syphilis should help to reduce the susceptibility for HIV infection, mainly among TW, their multiple sexual partners and clients.22

The marked variability in the prevalence of active and lifetime syphilis between TW and MSM reinforces the severity of the epidemic among TW group. In our country, many of the TW, who search for economic opportunities and freedom of sexual expression in a large city, are migrants from small cities, where high levels of discrimination prevail due to the dominance of conservative moral values. However, due to the difficulty of finding a job, poor education, discrimination and isolation, TW are extremely vulnerable to engaging in commercial sex work.23 ,24 Furthermore, their gender identity status overlaps with other vulnerabilities, such as poverty, high HIV/STIs prevalence, high levels of alcohol and drug abuse, depression and they are constant victims of violence and harassment.5 ,7 ,8 Indeed, both studied groups are stigmatised, but TW are more promptly identified due to their distinctive behaviour and physical appearance.23 ,24 This scenario may limit the access of these groups to healthcare services and prevention programmes, contributing to the high prevalence of syphilis infection.

This study was subject to several limitations. First, MSM and TW recruited from the streets and gay-related venues were sampled; therefore, the findings may not be representative of the larger community of these groups. Second, some risk behaviours may have been under-reported due to discrimination and stigma, leading to potential underestimation of associations with these variables and syphilis infection. Despite these limitations, our findings have important implications for future research and prevention efforts to improve and disseminate currently available strategies targeting MSM and TW in Brazil.

A large number of female sexual partners were reported and this variable remained independently associated with active syphilis among TW individuals. In addition, most TW reported to engaging in commercial sex work and had heterosexually identified clients who also have female partners (data not shown). Morineau et al6 found high levels of bisexual behaviour among MSM and high rates of inconsistent condom use with their female partners. Indeed, the bisexual behaviour of these groups may play a bridging role in the spread of syphilis from MSM/TW to general population, including uninfected female population, particularly due to elevated number of sexual partners and the lower level of condom use.6 On the other hand, the results of this study show that having a female partner is protective for active syphilis among MSM. This is consistent with a previous study conducted in Chinese MSM that reported frequent use condoms with female partners.25

The participants reported a variety of sexual practices. These sexual practices capture different levels of sexual experimentation and sexual adventurism and may serve as mechanisms to increase the risk for STIs transmission. It warrants mentioning that some of these sexual behaviours could be the potential risk for syphilis transmission in the presence of unprotected sex (e.g., rimming, group sex, shared sex toys). Furthermore, sexual practices such as fisting and use of sex toys may result in anorectal trauma and if followed by receptive unprotected anal intercourse within the same sexual episode could increase the risk of acquiring other pathogens.26 In this context, it is not surprising to find that sexual practices remained independently associated with lifetime syphilis among MSM. In addition, this study showed that participants also engaged in high rates of unprotected sexual intercourse with their partners and sex work clients, thereby creating even more opportunities for syphilis acquisition and transmission. Preventive interventions would encourage these groups to practice safer sex behaviours within different types of relationships and include educating men about potential risks associated with different sexual practices.

Although there was no statistically significant association between recreational drug use and syphilis infection in our study, the highest rate of recreational drug use was found among TW group. The majority of them were involved in commercial sex work. Prostitution may provide an opportunity to supplement income and allow them to sustain ongoing drug dependence.7 ,8 In addition, alcohol use was associated with active syphilis among MSM and this high level of alcohol consumption is also a reason for concern. Engaging in sex under the influence of alcohol and drugs decreases the ability to negotiate condom use with their sexual partner.6–8

Our study reported that MSM recruited on the massage parlour/sauna were at highest risk of active syphilis, which reflects the elevated and common behavioural risk factors adopted by these individuals. This finding suggests that more intensive control strategies should be targeted to these places through providing education materials, condom promotion, STI screening and treatment in order to reduce the potential risk of syphilis infection among this group. Our study also found predictors of high risk of lifetime syphilis infection included older age, multiple sexual partners, having been infected with HIV and history of genital/anal ulcer in the last 12 months. Important risk factors such as inconsistent condom use, drug use, lower education and history of sexual coercion were not associated with lifetime and/or active syphilis in this study. The lack of significant common and plausible risk factors for syphilis may reflect the relative homogeneity of the study population, especially among TW individuals. Studies with large sample size would contribute to a clearer picture of the most relevant risk factors for syphilis infection.

Currently, local campaigns and prevention efforts carried out by counselling and testing centres (CTA—Mato Grosso do Sul state) in partnership with the ONGs targeting MSM/TW have been performed in Campo Grande city. These have included testing for STIs, including syphilis, free provision of condoms and STI treatment services. The routine screening for syphilis is an essential part of HIV care in the public health programmes.27 However, the elevated prevalence of syphilis infection, including high VDRL titres suggestive of untreated infection, and risky sexual behaviour found in this study suggest that the current syphilis control programme should be re-evaluated. These programmes must urgently adopt effective measures for increasing the screening and detection of syphilis among MSM/TW in Brazil since the unspecific and painless syphilis symptoms can make diagnosis difficult. Additionally, health professionals need to be better trained to attend to the needs of these groups. Studies have shown that an automated text message and email reminders generated by computer to remind MSM/TW for syphilis testing at regular intervals could enhance the control of these infections.28 ,29 The regular serological screening of MSM/TW for syphilis could increase the detection rate of early syphilis and reduce the likely duration of infectiousness.

Our study revealed a high syphilis infection and sexual risk behaviours among MSM and TW groups. Despite the existence of HIV/STIs prevention programmes targeting these groups in our city, they continue to engage in sufficient syphilis-risk behaviour and have a substantial active infection rate. The findings suggest that syphilis is concentrated among MSM and among TW who predominantly engage in sex work. Finally, the differences in life experiences between MSM and TW highlight the importance of considering the unique characteristics of each group in targeting interventions.

Key messages

  • Our study revealed a high prevalence of syphilis infection and different sexual risk behaviours among men who have sex with men (MSM) and transgender women (TW).

  • The prevalence of syphilis infection was significantly higher in TW than in MSM.

  • Commercial sex work and drug use are common among TW.

  • High levels of bisexual behaviours and low rates of consistent condom use were observed in MSM/TW.

Acknowledgments

The authors acknowledge all the MSM and TW who participated in this study.

References

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Supplementary materials

  • Abstract in Portuguese

    This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

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Footnotes

  • Handling editor Jackie A Cassell

  • Contributors FRPF, PBZ, GRR, LSC and ARCMC were involved in the design and conducting of the survey. FRPF and ARCMC collaborated in the writing of the manuscript. LGB, LSC and LMB provided and checked the clinical data for patients. SAT performed the statistical analyses. ARCMC revised the manuscript before submission and complemented it with contextual data. LMB, MAP and TSOT did most of the laboratory work. All authors reviewed the draft and approved the final version.

  • Funding This study was support by FUNDECT-MS (n. 23/200.283/2009).

  • Competing interests None.

  • Patient consent Obtained.

  • Ethics approval The present study was approved by the Ethics Committee of the Federal University of Mato Grosso do Sul (n.158.931/2012).

  • Provenance and peer review Not commissioned; externally peer reviewed.

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