Introduction

In the recent years there has been increasing international attention on the relationship between migration and HIV/AIDS. Human mobility has constituted a general vehicle facilitating the global spread of HIV infection especially in Southeast Asia and sub-Saharan Africa (Beesey 2000; Day and Ward 1997). Poverty, anonymity, unemployment, lack of resources, social stigma, political and economic instability constitute factors leading to female sex work (FSW) worldwide, as well as migration (Ghys et al. 2001; McKeganey 1994). Immigrant FSW are vulnerable in their new environments for many reasons, including lack of familiarity/contact with legal systems, health regulations, immigration officers, and unfavorable workplaces (Duckett 2000). In addition, immigrant FSW may have higher rates of HIV/STI infection in comparison with local FSW, because they are often excluded or missed in prevention and medical care programs (Duckett 2000; Harcourt and Donovan 2005). Therefore, this mobile population represents a potential conduit for HIV/STI transmission and a bridge population between communities and countries (Ghys et al. 2001; Harcourt and Donovan 2005; McKeganey 1994).

The study of HIV and other STI-risk related factors has not been undertaken in immigrant FSW population to any great extent. Recently, limited studies in immigrant FSW populations have revealed positive behavioral changes in condom use for vaginal and anal sex among Asian FSW in Sydney (Pell et al. 2006) and consistent condom use among Latin American FSW in Madrid (Belza et al. 2004). However, HIV sexual risk behaviors and lack of knowledge regarding HIV/AIDS and its route of transmission were observed among migrant workers in Central America and Mexico (Bronfman et al. 2002), China (Bandyopadhyay and Thomas 2002) as well as in northeastern Brazil (Kerr-Pontes et al. 2004).

In South American countries, HIV infection levels among FSW populations varies very widely; higher rates of infection have been reported in Brazil, Argentina, Paraguay, and Ecuador, and to a lesser degree in Peru, Bolivia, Uruguay, and Chile (Montano et al. 2005; WHO/UNAIDS 2006). Data regarding the HIV-related risk behaviors among FSW in this region, especially as it relates to immigrant FSW are limited or do not exist. Therefore, we studied such epidemiologic risk factors by comparing immigrant (i.e., foreigner) with non-immigrant (i.e., local/native) FSW populations in Argentina, Bolivia, Ecuador, and Uruguay.

Methods

Participants and Procedures

HIV cross-sectional studies were conducted among FSW populations in the cities of Guayaquil in Ecuador, Santa Cruz in Bolivia, Buenos Aires in Argentina, and in six northeastern Uruguayan border cities with Brazil (Rivera, Chuy, Rio Branco, Bella Union, Melo, Artigas) during the years 1999–2002. details of the enrollment process, laboratory analysis, and preliminary results of the HIV epidemic have been described elsewhere (Bautista et al. 2006; Montano et al. 2005). Briefly, FSW who were at least 18 years of age were invited to participate by trained social workers and peer-risk group counselors at their working locations such as brothels, saunas, massage houses, parks, discos/bars, and on the streets. FSW were eligible for inclusion if they meet the UNAIDS definition of sex worker (UNAIDS 2002): women who receive money or goods in exchange for sexual services, either regularly or occasionally, and who may or may not consciously define those activities as income generating. The study sites were selected because of accessibility to FSW working locations and involvement by local NGOs and governmental agencies from each local Ministry of Health (MoH). The sampling performed was not based on a statistically-representative sampling of high versus low HIV prevalence areas in each country.

Participants were recruited after being given an explanation of study procedures, risks, and benefits of participants. After documentation of written informed consent, participants were asked to participate in a confidential face-to-face interview at their workplace, and then to provide a venous blood sample for HIV testing. No information on potential (i.e., participants approached) versus actual participants was collected.

Measures

A questionnaire in Spanish was developed to collect sociodemographic and epidemiologic data on sexual and drug-related risk behaviors. Participants were queried regarding their marital status, number of sex contacts a week, previous STI history, condom use with clients, time in sex work, main work place, illegal drug use habits, alcohol consumption, sex with foreign clients, and blood transfusion history. Participants received pre- and post-test counseling, and were referred to appropriate medical and social services for follow-up in accordance with local MoH guidelines. Following questionnaire completion, serum samples were collected and tested for antibodies against HIV-1 by ELISA screening (Bio-Rad, Hercules, CA). Repeatedly reactive samples were confirmed by Western blot assay (Calypte Biomedical, Alameda, CA).

Data Analyses

Chi-square and Fisher’s exact test were utilized to compare frequencies. The Mann–Whitney U test was used to compare means. Odds ratios were estimated to evaluate the association of risk factors for immigrant compared to non-immigrant FSW groups (i.e., local/native); age, number of sex contacts a week, condom use with clients, and illegal drug use were used in the adjusted multiple logistic regression analyses. All reported P-values were two-sided; P-values <.05 were considered statistically significant.

Results

Study Population

A total of 1,845 FSW participants were enrolled. Of these, 185 (10.1%) were immigrant FSW. A higher percentage of immigrant FSW was enrolled in Argentina (28.5%) and Uruguay (21.8%) (see Table 1). Most immigrant FSW in Argentina were from the Dominican Republic (39.3%), Paraguay (17.8%), and Uruguay (13.1%); in Bolivia most were from Ecuador (50.0%) and Brazil (33.3%); in Ecuador most were from Colombia (89.3%); and in Uruguay most were of Brazilian origin (97.0%).

Table 1 Distribution of FSW participants by country and immigration status in South America
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Statistically significant differences of demographic and risk behavior characteristics between non-immigrant and immigrant FSW were found for age group, previous STI history, time in sex work, use of illegal drugs, use of cocaine, and sex with foreign clients in Argentina (see Table 2); sex with foreign clients in Bolivia; age group, marital status, number of sex contacts a week, consistent condom use with clients, street as main work place, use of illegal drugs (marijuana and cocaine), use of alcohol, and sex with foreign clients in Ecuador; and time in sex work, use of alcohol and sex with foreign clients in Uruguay. In addition, time in sex work was significantly higher among non-immigrant Argentinean (10.0 vs. 5.1 years, Mann–Whitney U test = 4995.5, P < .01) and Ecuadorian FSW (4.3 vs. 2.4 years, Mann–Whitney U test = 8227.0, P < .05) in comparison with immigrant FSW.

Table 2 Demographic and risk behavior characteristics of FSW participants by country and immigration status in South America
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HIV Prevalence

Thirty-seven FSW participants were diagnosed with HIV infection. Of these, 34 were non-immigrant FSW (22 from Ecuador, 9 from Argentina, 2 from Uruguay, and 1 from Bolivia), and three were immigrant FSW (2 from Uruguay and 1 from Argentina). The overall HIV prevalence among immigrant FSW was 1.6% (95% CI = 0.3%−4.7%). The three immigrant HIV-infected FSW were of Brazilian origin, who worked in the cities of Buenos Aires, Rivera, and Chuy.

Risk Factor Analysis

Associations were estimated for immigrant (outcome) compared to non-immigrant (i.e., local/native) FSW (Table 3). Immigrant status was associated with younger age group (18–24 years old, [adjusted odds ratio] AOR = 10.81, 95% CI = 2.46−47.54) in Argentina; disco/bar as main work place (AOR = 7.70, 95% CI = 1.05−56.53) in Bolivia; single marital status (AOR = 5.40, 95% CI = 1.40−20.76) and use of illegal drugs (any, AOR = 20.81, 95% CI = 6.95−62.37; marijuana, AOR = 25.61, 95% CI = 7.73−84.87; and cocaine, AOR = 12.71, 95% CI = 1.61−100.29) in Ecuador; and brothel as main work place (AOR = 2.72, 95% CI = 1.05−7.02), use of alcohol (AOR = 2.25, 95% CI = 1.05−4.83), and sex with foreign clients (AOR = 109.07, 95% CI = 13.61−873.91) in Uruguay. On the other hand, higher time in sex work (≥6 years, AOR = 0.21, 95% CI = 0.12−0.38), use of illegal drugs (any, AOR = 0.32, 95% CI = 0.10−0.98), and sex with foreign clients (AOR = 0.37, 95% CI = 0.20−0.71) in Argentina, and a higher number of sex contacts a week (≥5, AOR = 0.16, 95% CI = 0.05−0.54) and consistent condom use (always, AOR = 0.07, 95% CI = 0.01−0.54) in Ecuador were inversely associated with immigrant status.

Table 3 Risk factors analyses for immigrant compared with local/native non-immigrant FSW participants by country in South America
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Discussion

This study provides insight into HIV-risk related sexual and drug use behaviors among immigrant (i.e., foreigner) and non-immigrant (i.e., local/native) FSW groups in South America. Our findings suggest that illegal drug use patterns were more common among immigrant FSW in Ecuador and Uruguay, and among non-immigrant FSW in Argentina.

In Argentina, commercial sex worker is illegal; therefore, those convicted may receive a jail sentence (of a few days), a fine, or both (Penal Code 1984). The high proportion of immigrant FSW enrolled in Buenos Aires possibly reflects the increase in sex tourism in this country and the opportunities for inexpensive sexual services afforded by Argentina’s depressed economy. Interestingly, illegal drug use was associated with Argentinean FSW. This association may be explained by the fact that this group of FSW might have high-risk sexual practices with IDU clients or with their IDU sexual partners.

In Bolivia, the number of immigrant FSW was insufficient to be able to conduct statistically-valid comparisons. The reason for the lower number of immigrant FSW is unclear. It is possible that this country does not constitute a sex tourism destination. On the other hand, disco was the main work place associated with immigrant FSW, which may suggests that this group prefers an environment with less exposure and more anonymity in order to avoid health inspectors and immigration officers.

In Ecuador, sex work is legal, and in recent years, this country has become a new destination in the Andean region for immigrant FSW. This has been stimulated by the so-called “dollarization” of its economy; the local currency (Sucre) is not longer accepted as a means of payment except for coinage, only US dollars are permitted as currency. Most immigrant FSW in this country were from the two neighbouring countries of Colombia and Peru, and most were in Guayaquil city (the main port of Ecuador, and a frequent commercial/tourist destination) (Carrion et al. 2003). According to MoH policies, FSW are required to have periodic check-ups for STI (every 2 months for syphilis and every 4 months for chlamydia) and HIV infections (every 6 months) (IBERB 2005). Most FSW are enrolled during their visits to clinic health centers, however, street sex workers, who are usually poorer and older, are less likely to be part of this enrollment. In our population, a significant proportion in both non-immigrant and immigrant FSW indicated the streets as their main workplace. However, non-immigrant FSW reported more sexual contacts per week and low rate of condom use with clients, putting them at a high risk for HIV/STI infection. A recent study reported that local FSW had more clients than international (i.e., immigrant) FSW in Sydney, Australia (Fox et al. 2006). On the other hand, illegal drug use was higher among immigrant compared to non-immigrant FSW, despite the small number in this group (2.7%, 28 of 1,047). A complex and mutually reinforcing relationship between drug use and prostitution has been previously reported (Miller 1995; Potterat et al. 1998).

In Uruguay, most immigrant FSW were of Brazilian origin and reported a high number of sexual contacts with foreign clients. This may be explained by the geographic location where participants were enrolled (in eastern border cities with Brazil). The relatively short geographic distances and the ease of travel between these countries contributes to the migration of Brazilians FSW to Uruguay and Argentina. In addition, immigrant FSW also reported higher alcohol consumption, which coincides with predominantly poorer working locations. A recent study conducted in the cities of Beijing and Nanjing in China among 1,543 female migrant sex workers indicated that employment conditions were associated with HIV risk (Yang et al. 2005).

Among immigrant FSW in Ecuador and Uruguay, condom use with clients was higher and a previous STI history was lower compared to non-immigrant FSW. These findings suggest that immigrant women were healthy when they arrived in Ecuador and Uruguay and condom use, one of the most important preventive measures to reduce HIV/STI transmission (Foss et al. 2004; NIAID 2002) is highly practiced among immigrants. Similar findings have also been reported among Colombian and Dominican FSW in Catania, Italy (Nigro et al. 2006). In addition, in our study population, few non-immigrant FSW reported ever having used injecting drugs. The low rate of injecting drug use was also reported among 579 Latin American FSW in Madrid (Belza et al. 2004).

Positive relationships with use of illegal drugs (any, marijuana or cocaine) as well as sex with foreigners were observed among immigrant FSW in Ecuador and Uruguay. However, these factors were found to be inversely associated with immigrant status among FSW in Argentina. In addition, younger age group (18–24 years old) and single marital status were observed to have a positive association with immigrant status among FSW in Argentina, Ecuador, and Uruguay. The role that these different risk factors play in terms of association with immigrant status among FSW in the region is unclear at this point.

We recognize that our study has some limitations. First, it is possible that more established immigrants FSW were underrepresented because of our data collection methods; the non-representativeness of the sample population might narrow the external validity of the study findings. Second, we could not objectively assess the role of other unmeasured risk sexual behaviors (e.g., fee per sexual contact or receptive anal intercourse) for HIV/STI acquisition or transmission. Third, the size of the observed effects (odds ratios) could be reduced with some true associations undetected because of the small number of immigrant participants in our study. Further work with adequate sample size is required to determine more reliably the size of effect as well as to clarify the presence and direction of the relationships in order to compare differences between immigrant and local/native FSW. Nonetheless, we believe these data have important implications for HIV/STI prevention efforts, among marginalized FSW in South America. The present study needs to be expanded to more objectively evaluate associated risk factors for STI, including HIV infection.

In conclusion, use of illegal drugs (especially marijuana and cocaine) were associated with Argentinean FSW and with immigrant FSW in Ecuador. Harm-reduction intervention programs may be necessary to address this problem in these high-risk groups/countries and must be tailored to local conditions. In Uruguay, immigrant FSW were observed to have higher alcohol consumption, which coincides with predominantly poor working locations (discos/bars). On the other hand, inconsistent condom use with clients among non-immigrant FSW in Bolivia, Ecuador, and Uruguay suggest additional avenues for public health interventions. Finally, immigrant FSW groups have specific local country needs with respect to STI and HIV/AIDS prevention and care. Therefore, interventions should take into account their cultural, social, and economic backgrounds.