Male Sex Workers in Lisbon, Portugal: A Pilot Study of Demographics, Sexual Behavior, and HIV Prevalence

HIV transmission among men who have sex with men (MSM) is a major concern in Portugal, since MSM remain one of the most at risk groups for HIV transmission [1,2]. However, little is known about HIV transmission and sexual practices among male sex workers (MSW) who work with male clients in Portugal, particularly in Lisbon. Male sex workers (MSW) are thought to be at an increased risk of sexually transmitted infections (STIs), since some STIs are more prevalent and reinfections are more common among MSWs than in other groups of men, including MSM [3,4].


Introduction
HIV transmission among men who have sex with men (MSM) is a major concern in Portugal, since MSM remain one of the most at risk groups for HIV transmission [1,2]. However, little is known about HIV transmission and sexual practices among male sex workers (MSW) who work with male clients in Portugal, particularly in Lisbon. Male sex workers (MSW) are thought to be at an increased risk of sexually transmitted infections (STIs), since some STIs are more prevalent and reinfections are more common among MSWs than in other groups of men, including MSM [3,4].
It has been demonstrated that entry into the sex work industry is linked to economic and emotional factors, making it difficult to exit sex work and establish goals. Additionally, links between economics and beliefs influence MSWs' perceived HIV/STI risks, vulnerability, and prevention practices [5]. The current social and economic circumstances in Portugal, shaped by the financial crisis and the growing acceptance of same-sex forms of sexual recognition, including same-sex marriage, [6] have been accompanied by an increase indifferent forms of sex work. The proliferation of sex work was in part an adaptive response to the loss of previous income, but was also facilitated by changing social norms that increased the supply side for sex work. This has occurred mainly in Lisbon, the capital of Portugal, where prostitution was decriminalized in 1983, but there is still a political void concerning sex work, as there is no professional recognition by the state [7]. Despite this, sex work in general, and male sex work in particular, is strongly socially reproved [8]. This stigma may partially explain why so little information is known, relegating MSW in Portugal to an invisible place in society and leaving them vulnerable to discrimination.
According to the European Centre for Disease Prevention and Control [9], HIV prevalence among MSW in Portugal is 13.5%, one of the highest rates in Western Europe. Another Portuguese study concerning MSW indicated a rate of 5% [10], reflecting the need for more accurate studies of this population.
Regarding the socio-demographic characterization of MSW, few studies exist that give an accurate idea of their social profile. Most studies look for determinants of entrance into the sex industry, such as personality characteristics, alcohol and drug abuse, lack of job opportunities, academic problems, depression, and violence [11]. These studies also focus on the professional consequences of sex work, such as: professional isolation, threats to personal safety, limited perceived HIV risk, and sub-optimal levels of condom use [12]. Previous studies have also examined other general determinants, such as family factors, sexual and criminal history, and current life situation, sexual practices with clients, financial gain, sexual orientation, and early sexual experiences [13]. Furthermore, the majorities of MSW are generally young and are working in the sex industry for the first time after immigrating to the city where they do their sex work [14].
When it comes to understanding sexual behavior among MSW most studies are inconclusive. Results vary widely, as some studies have found that condom use is inconsistent for receptive and insertive anal intercourse, especially when associated with lower education, fear of HIV infection, and a history of sexually transmitted infections [15].
However, other studies have demonstrated that around 87% to 100% of MSW consistently use condoms for anal intercourse with their clients [4,9].
Therefore, HIV infection in MSW needs to be understood in conjunction with its psychosocial correlates and sexual practices. This research was conducted as there are no prior studies that have examined MSW in Lisbon, Portugal, who are at an especially high risk for HIV infection. While MSW are an important population to characterize, they are also a challenging group to identify and follow in Portugal, rendering this study even more pertinent.

Participants and procedures
A total of 143 MSW participated in this research. Participants were generally young with the majority being under the age of 28 (mean age=28.26, SD=5.96). Only 21% of the participants are originally from Portugal. The majority was Brazilian immigrants, and the vast majority of recruited MSW engaged in sex work indoors (94.4%). About 68% reported being unemployed and sex work was their primary source of income. Financial reasons or the lack of better employment opportunities were cited as the primary reasons for their entry into sex work. See Table 1 for more information on demographic characteristics of the sample.
The research was part an outreach program called "Encontros (In) Seguros" ((Un) Safe Encounters) which was aimed at preventing HIV and other STIs in MSW. Encontros (In) Seguros was conducted by the Portuguese League against AIDS (Liga Portuguesa Contra a SIDA), a non-governmental organization committed to expanding HIV prevention efforts in Portugal. Participants were recruited through team visits to indoor sex work facilities, namely apartments, where the opportunity was taken to distribute information, condoms, and lubricant gel. Rapid HIV tests were made available by the team to control the serostatus of all participants. This outreach program took place between 2011 and 2013.

Materials
Demographic characteristics: Data on participants' age, sexual orientation, nationality, marital status, educational attainment, employment, sex role, and the venue where sex work was conducted (indoor or outdoor) were collected. For the purpose of data analysis, all variables were grouped into several categories.

HIV-related sexual behavior:
HIV-related sexual behavior was operationalized using a measure created for this study. Participants were instructed to respond to the following items regarding sexual behavior with clients: gender of client, frequency of condom use in oral sex, anal sex, and vaginal sex (never, rarely, almost always, always or doesn't apply), if a condom was used with the last client, and if condom use is discussed when a client refuses to use one. Regarding sexual behavior with partners, the following items were added: if a condom was used in the last sexual relationship with their partner and if a condom was used in the last anal sexual relationship with their partner.
HIV history and testing: a short-form questionnaire regarding HIV testing history (prior to rapid testing) was used. It included 2 questions: "How often do you test for HIV?" (Never tested; every 3 months; every 6 months; once a year; every 2 years or more), and "Have you had an HIV test in the previous year?"(Yes or no). Rapid HIV testing was done using commercially available and legally approved rapid test kitsin Portugal.

HIV related Sexual behavior with clients
Most participants said that they worked on a daily basis, having 4 clients a day (average number of daily clients=4.08; SD=2.27), and 82.5% have exclusively male clients. Table 2 shows that nearly 70% of MSW say that they use condoms in oral sex, and 95.1% in anal sex. 2.1% said that they didn't use a condom with a client in the last sexual relation, and 4.2% said that they didn't discuss the use of condom when a client refused to use one. Table 3 shows the results for sexual behaviors with their partners. A plurality of respondents (44.8%) said that they had sex with only one sexual partner, 68.5% of whom were male. Nearly 20% said that they never use condoms for anal sex with their partners, and 47% never use condoms for oral sex. Results also show that 32.2% did not use a condom in their last sexual relationship, and 21% did not use a condom for anal sex.

HIV history
Regarding HIV history, the majority said that they were tested every 6 months or once a year (39.2% and 32.9% respectively). Nevertheless, 9.1% of all MSW said that they had never been tested, and 21.7% of participants had not been tested during the past year. Results of HIV rapid testing showed that the prevalence of HIV infection was 8.4% (Table 4).
When comparing HIV testing patterns and results by sexual orientation and sexual position, results show that self-identified gay MSW have been tested for HIV more frequently over the previous year than bisexual and heterosexual self-identified MSW, and that this difference was statistically significant (p=0.020). Yet, no differences were found regarding the relationship between sexual orientation and HIV serostatus (Table 5). When comparing HIV testing patterns and HIV results by sexual positions, our results indicate that MSW who said that they were versatile were tested much more often over the previous year than those who said that had insertive or receptive anal intercourse, and that this difference was also significant (p=0.026). No statistical differences were found between sexual positions and HIV serostatus results despite the fact that more HIV positive MSW were versatile (Table 6).

Discussion
The main objective of this study was to assess the prevalence of HIV and behavioral circumstances in a sample of 143 MSW using outreach team members of the (UN) Safe Encounters project. In this study, HIV prevalence was found to be 8.4%, and MSW reported low levels of HIV risk behavior when having sex with their clients; however, this was not the case for sexual practices with their partners. Given the background of HIV prevalence in this group, MSW are at high risk of acquiring and transmitting HIV. Risk factors included inconsistent condom use with their partners during receptive anal, oral and vaginal intercourse. Studies have demonstrated that having a condom available at all times increases the likelihood of its use when sexual intercourse occurs [16,17]. Alternatively, possession of a condom may be an indicator of being better informed and of the willingness to use a condom when necessary. In our study MSW were more likely to carry a condom at the time of the survey, because condoms, as well as support and information regarding HIV and AIDS, were made available by the team. This finding demonstrates the importance of targeting MSW venues more often with outreach activities, especially the distribution of condoms and information. Other studies of MSWs confirm higher levels of condom use than among other at-riskgroups [18].
This study also found that the majority of MSW working in Lisbon were Brazilian immigrants who live away from their family or from their primary sources of social and emotional support. Additionally, they were more likely to use condoms inconsistently when having anal intercourse [19]. As it has been suggested, it is possible that men living away from their families have lower social support levels and fewer financial means to negotiate condom use effectively with partners, particularly if there is an obligation to support their extended families at home [20].
Being versatile during anal intercourse (or being both receptive and insertive) with a partner was found to be associated with inconsistent condom use among MSW. The decreased control versatile partners have over condom use compared with exclusively insertive or receptive partners may contribute to this risk, thus making versatile MSW test more for HIV. Moreover, versatile MSW were more likely to be HIV positive than MSW who said that they had exclusively insertive or receptive anal sex. Therefore, programs aiming to increase consistent condom use in MSM and MSW should address the responsibilities of both partners in anal intercourse and should include strategies for increased condom negotiation skills and the ability to carry out safer sexual scripts with partners to effectively negotiate condom use [21,22]. In light of the group-specific risk factors highlighted in the analysis, this information can beused to design HIV prevention messages that are applicable to MSM in general and various at risk subgroups.
Low levels of consistent condom use among MSW reflect recent trends in condom use among the broader population of MSM. Because MSM and MSW are more likely to be infected with HIV in Portugal [23,24], the epidemic has the potential to spread further in this population. These epidemiologic factors combined with the difficulty of reaching this target population signify the need for HIV prevention initiatives specific to MSW.
Our study demonstrated high levels of consistent condom use with clients among MSW; however, it had its limitations. Importantly, the risk behaviors of our sample may not be representative of the total population of MSW since participants were recruited from venues (apartments) where men socialize and find clients, in addition to having access to outreach and prevention materials such as condoms and lubricant. Levels of consistent condom use and risk behavior may be overestimated because MSW who gather in indoor venues may have higher risk profiles. The fact that measure used has not been validated, but was created for the study, is also a potential limitation of the study. At the same time, this is done in other qualitative/community-based participatory research as the measures are made specifically for the community group under study and meant to be representative of their specific and unique characteristics and behaviors. On the other hand, participants in our study may have over-reported the use of condoms, because they may be aware that this is the normative response.
The HIV epidemic has not been well controlled among MSM in Portugal [20]. The consistent condom use with clients among a large percentage of MSW, but the inconsistent condom use with partners, suggests that the spread of HIV will not decrease until we observe widescale behavioral change among these groups, especially within romantic relationships with partners. Future studies may consider assessing the partners of MSWs to obtain additional dada on this topic.
Finally, qualitative studies to increase and deepen our understanding of the reasons that MSW in Portugal cite for not using condoms consistently are also urgently needed. To maximize efficacy, HIV prevention campaigns must be able to consistently have access to and adequately monitor this invisible population of MSW.