Male and transgender women sex workers (TSWs) are worldwide considered as a high-risk population for sexually transmitted infections (STIs) and human immunodeficiency virus (HIV).1–6 They are known to engage in high risk sexual behavior, such as having multiple sex partners with unknown HIV status and condomless anal sex (CAS).1,2,4 In different countries, substance use among male and TSWs was associated with high-risk sexual behavior.1,4,7–10 Consistent among different studies, substance use among male and transgender sex workers was considered a relevant contributing factor for sexual risk behavior.1,6,10 Dias and colleagues11 showed that a reported HIV infection was higher among transgender who ever used psychoactive substances. Most of the studies, however, looked at injecting substance use among male and transgender sex workers.1,4,7–9 Thus, data regarding a broader use of psychoactive substances among sex workers during sex with their clients and with their nonpaying partners are limited. Besides, previous studies emphasized the importance to distinguish TSWs from male sex workers due to their differences in biological and structural risk factors.1,4 We, therefore, looked in detail at sex work-related substance use and distinguished between TSWs and male sex workers.12 Because male-male sexual contact is associated with increased STI risk compared with heterosexual contact, we looked separately within the group of male sex workers between those having sex with men and those exclusively having sex with females.13 Here, we aimed to assess the sociodemographic, sexual health, and work-related substance use characteristics among distinctive groups of male and transgender sex workers.
MATERIALS AND METHODS
Visitors of the Prostitution and Health Center
The Prostitution and Health Center (P&G292) in Amsterdam opened its doors in 2008 with the aim to provide sexual health care for sex workers at a clinic located near the Red-Light District. P&G292 is a collaboration of the Public Health Service of Amsterdam (offering sexual and other health care) and HVO-Querido (offering social work). P&G292 is a specialized care facility for male, female, and transgender sex workers offering information, advice, and support from social workers (eg, social services such as financial help, issues around health insurance, rights as sex workers) as well as STI testing and sexual health counseling. Next to sex workers, who request a consultation at P&G292, it is a standard practice to approach sex workers online, in sex clubs, and in the red light district (window prostitution) via outreach activities.
Routinely Collected Data of All Visitors of P&G292
We retrieved data from the electronic patient files (EPD) of all sex workers (male, female, and transgender) who visited P&G292 between January 2014 and December 2015. Routinely collected data were age, ethnicity (western vs. nonwestern, ethnicity was defined according to Statistics Netherlands on the basis of country of birth, maternal and paternal countries of birth),14 reason of visit (symptoms or being notified of an STI by a sex partner), HIV status, sex of sex partner(s), CAS, and condomless vaginal sex in the previous 6 months and the number of sex partners in the previous 6 months. Also, clinical outcomes of bacterial STIs (chlamydia (including lymphogranuloma venereum [LGV]), gonorrhea, infectious syphilis), syphilis serology, and new HIV diagnoses were retrieved from the EPD and analyzed among all groups of sex workers.
Participants of the Study
Only male and TSWs who had an STI consultation at P&G292 in the study period were asked to participate in the study and participate in a questionnaire-based interview (female sex worker [FSW] were not included).
The study population was divided into 3 subpopulations; 1) men having sex with men only or also with females (MSW-M), 2) TSWs (those assigned male at birth who identify themselves as women) (TSW) and 3) men having sex with females only (MSW-F). We included transgender women who were assigned male at birth and had not undergone genital reconstructive surgery.
Questionnaire Data on Substance Use and Work-Related-Sexual Behavior
All MSW and TSW who participated in the questionnaire-based interview were asked by a health care worker from P&G292 about their sexual (working) career, work-related sexual (risk) behavior, substance use, and reasons for substance use during working time. The reasons for substance use were registered by 9 different response options and also with a write in option. The use of the following substances in the previous 6 months was scored: (1) illicit substances: cocaine (snuff coke), XTC (Ecstasy)/MDMA, ketamine, mephedrone, GHB/GBL, amphetamines, methylamphetamine; and (2) tolerated substances: erectile stimulation drugs, nitrites, marihuana (not an illicit substance in the Netherlands), and/or alcohol. Moreover, they were asked in which context these substances were used: during sex work, during sex, but not work-related, and/or not sex related. Work-related sexual (risk) behavior was scored as engaging in condomless oral sex (COS) (insertive and/or receptive) and CAS (insertive and/or receptive) in the previous 6 months with clients. Work-related condomless vaginal sex was not asked. All EPD data were merged with the questionnaire data and were anonymized afterward.
The study protocol was evaluated by the Medical Ethics Committee of the Academic Medical Center in Amsterdam (letter reference no. W13_308) and deemed not to require a full review of the board because the emotional impact of the additional questionnaire was considered negligible.
STI Testing Procedure
Sex workers were tested for Chlamydia trachomatis (Ct) (including LGV in case of anorectal Ct in MSW and TSW), Neisseria gonorrhoeae (Ng), and syphilis. All sex workers who had not previously tested HIV-positive were tested for HIV unless they actively opted out.
Urine, pharyngeal, rectal, and vaginal specimens were tested for both Ct and Ng with the Aptima Combo 2 assay (Hologic, Marlborough, MA). In asymptomatic visitors both urine, rectal, and vaginal specimens were self-collected, while in symptomatic visitors medical staff collected rectal specimens. Medical staff collected pharyngeal specimens in all sex workers. The HIV antibodies were tested with the HIV Ab/Ag test (LIAISON XL; Diasorin, Saluggia, Italy), and a treponemal test for syphilis serology was performed with the Treponema Screen (LIAISON XL; Diasorin, Saluggia, Italy). All bacterial STI diagnoses were based on laboratory outcomes of the STI consultation in which the substance questionnaire was taken.
During the study period, the first consultation of a visitor of P&G292 was used for the analyses. All routinely collected data from the EPD of all sex workers who visited P&G292 during the study period were compared with the χ2 test for independence, the Fisher exact test, and the Mann-Whitney U test. With the abovementioned statistical tests we compared the STI positivity, sociodemographic characteristics, sexual behavior, and substance using behavior retrieved by the additional questionnaire between the 3 substudy populations (MSW-M, TSW, MSW-F).
Age was divided into 4 categories.15 The HIV status was divided into HIV-negative including visitors who refused an HIV test, and HIV-positive. Data analyses were performed with SPSS package v21.0 (SPSS, Chicago, IL). In the present study, a P value less than 0.05 was considered statistically significant.
Visitors of P&G292
Between January 1, 2014, and November 19, 2015, 1557 unique male, female, and transwomen sex workers had an STI consultation at P&G292 (Fig. 1) with a total of 3631 consultations. Of those 1557 sex workers, 6.4% were MSW-M, 2.6% were TSW, 1.6% were MSW-F, and 89.5% were FSW (Table 1). TSW were significantly older compared with the 3 other groups (median age: MSW-M 28 vs. TSW 43 vs. MSW-F 29 vs. FSW 28; P < 0.001). The groups also differed significantly regarding their ethnicity (nonwestern: MSW-M 62.2% vs. TSW 87.5% vs. MSW-F 60.0% vs. FSW 78.3%; P < 0.001). Only among MSW-M (5/28;6.1%) and FSW (4/1356;0.3%), new HIV diagnoses were found. Bacterial STI positivity was among MSW-M 31.3% versus TSW 25.0% versus MSW-F 12.0% versus FSW 10.0% (P < 0.001).
Of all male and TSWs who were asked to fill in the questionnaire, 60.4% (n = 99/164) participated in the present study of whom 69.7% were MSW-M, 15.2% were TSW, and 15.2% were MSW-F (Supplement 1, https://links.lww.com/OLQ/A434). Participants were significantly younger (median: 29 years vs. 34 years; P = 0.036), more often western (38.4% vs. 21.5%; P = 0.026), and less often transgender women (15.2% vs. 38.5%; P < 0.001) compared with nonparticipants. Participants did not differ from nonparticipants regarding STI positivity, HIV status, number of sex partners, and CAS in the previous 6 months.
Demographics and Sexual (Risk) Behavior of Study Participants
Transgender women sex workers in our study were significantly older (median age: MSW-M 28 vs. TSW 39 vs. MSW-F 29; P < 0.001) (Table 2). More than half of the participants in all 3 groups were of nonwestern ethnicity (MSW-M 59.4% vs. TSW 73.3% vs. MSW-F 60%; P = 0.658). Transgender women sex workers reported the highest number of sex partners in the previous 6 months (median: MSW-M 60 vs. TSW 300 vs. MSW-F 12; P < 0.001) compared with MSW-M and MSW-F (Table 2). No significant differences in the proportion who engaged in CAS or COS were found. Of all TSW, 80.0% reported solely sexual contact with men (during work and private), whereas only 50.7% of the MSW-M reported sex solely with men. Most MSW-M got in contact with their clients online (81.2% vs. TSW 33.3% vs. MSW-F 40.0%; P < 0.001), whereas 66.7% of TSW worked in window prostitution (MSW-M 2.9% vs. MSW-F 0%; P < 0.001). Most sex workers reported working at least once a week (MSW-M 83.8% vs. TSW 100% vs. MSW-F 80.0%; P = 0.85).
STI and HIV Diagnosis of Study Participants
Bacterial STI positivity was 29.0% in MSW-M, 26.7% in TSW, and 13.3% in MSW-F (P = 0.56) (Table 2). Syphilis serology was positive in 21.7% of the MSW-M, 53.3% of the TSW, and 0% of the MSW-F (P = 0.002). None of the MSW-F were known HIV-positive, whereas 20.3% of MSW-M and 20.0% of TSW were known HIV positive (P = 0.14). Only in the group of MSW-M, new HIV infections were diagnosed (n = 3; 5.2%).
Substance Use Characteristics
Overall, 65.2% of the MSW, 60.0% of all TSW, and 35.6% of MSW-F used illicit substances in the previous 6 months, either during work or free time (Table 3). During work, 40.5% of the MSW-M and 40.0% of all TSWs used illicit substances, whereas 20.0% of MSW-F used illicit substances (P = 0.02). Cocaine was used in 45.6% of all sex workers. Notably, 21.7% of all MSW-M and 26.7% of all TSW used cocaine during work only. Other substances that were often used during work only were nitrites (MSW-M 24.6% vs. TSW 40.0% vs. MSW-F 6.7%; P = 0.07) and erectile performance drugs (MSW-M 50.7% vs. TSW 26.7% vs. MSW-F 53.3%; P = 0.22). XTC was mostly used during free time only and hardly during working time. Chemsex (with associated substances GHB/GBL, mephedrone, and/or methylamphetamine) was almost only practiced by MSW-M (27.5% vs. TSW 6.7% vs. MSW-F 6.7%; P = 0.88) and 5.8% of all MSW-M reported chemsex during working time only.
Reasons for Substance Use During Work
Sex workers reported several reasons for substance use during work. The most reported reason, regardless of the subpopulation, was that “sex work becomes physically easier” (MSW-M 48.4% vs. TSW 55.6% vs. MSW-F 28.6%; P = 0.36) (Table 3). The reason “the client asked for it” was the second most by MSW-M, and the first most frequently named reason by TSW (MSW-M 37.1% vs. TSW 55.6% vs. MSW-F 7.1%; P = 0.27). Other frequently reported reasons were “work becomes mentally easier” and “I dare to do things I would otherwise not dare.” Dependency as reason for using substances during work was mentioned in 4.8% of MSW-M, in 11.1% of TSW and in 7.1% of MSW-F (P = 0.41). Two TSW and 7 MSW-M filled in the write in option for this item. Their answers were: “I make more money,” “works against stress,” “for my erection,” “for social feeling,” “to calm down,” and “for fun.”
Substance Use and STI Positivity
The bacterial STI positivity among sex workers using illicit substances during working time was 17.9% (5/28) among MSW-M, 50.0% (3/6) among TSW, and 0% (0/3) among MSW-F (P = 0.21) (Table 4). Among MSW-M and MSW-F, illicit substance use during working and/or free time was not associated with an STI diagnosis. Among TSW, a significant association (P = 0.04) of illicit substance use and STI positivity was found.
We found discerningly high-risk sexual behavior and substance use among MSW and TSW in Amsterdam, the Netherlands. All 3 study groups (MSW-M, MSW-F, and TSW) differed concerning demographics, sexual risk behavior, and substance use. Nonetheless, almost half of all sex workers reported CAS with clients and/or private sex partners and most of all sex workers reported illicit substance use. By differentiating MSW based on the sex of their clients, we were able to distinguish differences in risk behavior between MSW-M and MSW-F. Our study showed a high bacterial STI positivity particularly among MSW-M (29.0%), and TSW (26.7%) visiting the Prostitution and Health Centre P&G292 in Amsterdam.
The 3 groups also differed significantly in substance use during work: MSW-M (40.5%) and TSW (40.0%) most frequently reported work-related substance use as opposed to MSW-F (20.0%). Also, working time only related use of cocaine was reported frequent among MSW-M (21.7%) and TSW (26.7%).
As motivation for work-related substance use, all sex workers reported most often that “sex work becomes physically easier.” Interpreting this as risky behavior and a short-term solution to endure their work, can be explained by Sosa-Rubi and colleagues16 who found that those male sex workers more inclined toward the present perspective than the future perspective tended to engage in more risky sexual behavior. The second most often-reported reason for substance use during work by MSW-M and most often-reported reason by TSW was that “the client asked for it.” This was also described by Galárrae et al17 who found that male sex workers get paid higher prices by their clients for risky sexual behavior.
Surprisingly, few sex workers (5.9%) reported dependency as reason for substance use during work, whereas around 45% reported cocaine use (private and/or work-related) which is known to be a highly addictive substance and associated with sexual risk behavior.18 Participants' possible underestimation of drug dependency is worrying if it hinders their motivation to enter substance use programs.
We found that 50% of TSW and 17.9% of MSW-M who used substances during work had a bacterial STI diagnosis. In contrast, none of the MSW-F using substances during work were infected with a bacterial STI, confirming earlier reports on the increased risk for STI transmission in male-male sexual contact.13 Only among TSW, we found a significant association (P = 0.04) of illicit substance use and STI positivity.
As already stated by Poteat et al,4 we confirmed the importance to distinguish TSW as a separate group from other male sex workers regarding their sexual (risk) behavior. TSW reported 5 times more sexual partners in the previous 6 months than MSW-M and even 25 times more sex partners than MSW-F. One possible explanation is that these TSW more often engaged in window prostitution, which allows for more clients compared with the other groups who have to rely on other ways to seek clients such as dating sites.
The proportion of TSW who were known HIV-positive (20.0%) was comparably high to MSW-M (20.3%). This is also in accordance with previous studies in the Netherlands and a systematic review by Baral et al2,6 who found a pooled HIV prevalence of 19.1% among all transgender women worldwide. Comparable figures were found among sex workers who declined participation (Supplement 1, https://links.lww.com/OLQ/A434). The 3 new HIV infections were all diagnosed among MSW-M. In contrast with the comparable HIV prevalence, syphilis serology was more often positive among TSW (53.3%) than among MSW-M (21.7%). High syphilis serology rates among transgender persons were also described by Zoni et al19 in a systematic review among at-risk populations in Latin America and the Caribbean (compared with MSM, MSW, and FSW).
Strengths of this study are the routinely collected and laboratory confirmed STI data, and detailed sociodemographic, (sexual) behavioral data as well as detailed information on drug use during sex work. Previous studies had to rely on self-reported STI diagnoses.11 Moreover, by subanalyzing all sex workers in separate groups (TSW, MSW-M, and MSW-F), the surprising differences in risk behavior and substance use between these populations underline the importance of acknowledging nuances, such as the sex and gender of sex workers, as well as their clients.1,4 Our results can help to formulate tailor-made care for subpopulations of sex workers. Another strength of the present study is that we described a group that engaged in sex work frequently (ie, more than 85% reported to work at least once a week). This is in contrast to earlier studies including men who just every now and then have sex in exchange for goods or food and do not recognize their practice as a regular income-generating activity.1
Our study also has some limitations. Due to the small sample size of our study, the findings should be interpreted with caution. However, studies involving MSW and TSW are often hampered by small numbers, emphasizing the difficulty to recruit members of these key populations. Earlier studies from Baral et al1 likewise report on small samples of MSW and TSW. Moreover, our findings apply to the Dutch situation where sex work is legal. In settings where sex work is criminalized, other outcomes can be expected. Lastly, we lack data on poly substance use, frequency, and amount of substance(s) used, and we cannot specify the reason for substance use for each substance separately.
Future research on sexual risk behavior in relation to substance use among MSW and TSW should invest in recruiting larger samples of TSW and MSW. Moreover, in-depth qualitative research is needed to better understand the intentions and reasons for substance use during work and the effect of substance use on risk behavior and daily life.
To our knowledge, we present the first study describing the sociodemographic characteristics, sex work-related substance use characteristics, and STI diagnosis of male and transwomen sex workers in the Netherlands. Moreover, our study distinguishes between different groups of sex workers as suggested by earlier research.1,4 The present results demonstrate that MSW-M and TSW sex workers are at high risk for STIs and HIV, considering the high proportion that are known HIV positive, and the newly diagnosed HIV infections among MSW-M. Therefore, biomedical interventions, such as pre-exposure prophylaxis, should be offered actively to MSW-M and TSW.20 Only a minority acknowledges drug dependency which is possibly an underestimation because a large number of sex workers use highly addictive substances, health services working with MSW-M, and/or TSW should consider to implement substance counseling services and offer referral to substance use clinics once motivated.
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