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AIDS Care: Psychological and Socio-medical Aspects of AIDS/HIV Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/caic20
HIV seroprevalence and high-risk sexual behavior among female sex workers in Central Brazil a
a
a
a
Fernanda R.P. Fernandes , Gina J. Mousquer , Lisie S. Castro , Marco A. Puga , Tayana S.O. a
a
a
a
b
Tanaka , Grazielli R. Rezende , Clarice S. Pinto , Larissa M. Bandeira , Regina M.B. Martins , c
d
Roberta B.L. Francisco , Sheila A. Teles & Ana R.C. Motta-Castro
a
a
Department of Biochemistry and Pharmacy, Federal University of Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil b
Institute of Tropical Pathology and Public Health, Federal University of Goiás, Goiânia, Brazil
Click for updates
c
Central Public Health Laboratory, LACEN/MS, Campo Grande, Brazil
d
School of Nursing, Federal University of Goias, Goiânia, Brazil Published online: 12 Mar 2014.
To cite this article: Fernanda R.P. Fernandes, Gina J. Mousquer, Lisie S. Castro, Marco A. Puga, Tayana S.O. Tanaka, Grazielli R. Rezende, Clarice S. Pinto, Larissa M. Bandeira, Regina M.B. Martins, Roberta B.L. Francisco, Sheila A. Teles & Ana R.C. Motta-Castro (2014) HIV seroprevalence and high-risk sexual behavior among female sex workers in Central Brazil, AIDS Care: Psychological and Socio-medical Aspects of AIDS/HIV, 26:9, 1095-1099, DOI: 10.1080/09540121.2014.894609 To link to this article: http://dx.doi.org/10.1080/09540121.2014.894609
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
AIDS Care, 2014 Vol. 26, No. 9, 1095–1099, http://dx.doi.org/10.1080/09540121.2014.894609
HIV seroprevalence and high-risk sexual behavior among female sex workers in Central Brazil Fernanda R.P. Fernandesa*, Gina J. Mousquera, Lisie S. Castroa, Marco A. Pugaa, Tayana S.O. Tanakaa, Grazielli R. Rezendea, Clarice S. Pintoa, Larissa M. Bandeiraa, Regina M.B. Martinsb, Roberta B.L. Franciscoc, Sheila A. Telesd and Ana R.C. Motta-Castroa a
Department of Biochemistry and Pharmacy, Federal University of Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil; Institute of Tropical Pathology and Public Health, Federal University of Goiás, Goiânia, Brazil; cCentral Public Health Laboratory, LACEN/MS, Campo Grande, Brazil; dSchool of Nursing, Federal University of Goias, Goiânia, Brazil b
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(Received 9 May 2013; accepted 11 February 2014) Female sex workers (FSWs) are considered a high-risk group for human immunodeficiency virus (HIV) infection due to their social vulnerability and factors associated with their work. We estimated the prevalence of HIV, and identified viral subtypes and risk factors among FSWs. A cross-sectional study using respondent-driven sampling (RDS) method was conducted among 402 FSWs in Campo Grande city, Brazil, from 2009 to 2011. Participants were interviewed using a standardized questionnaire about sociodemograpic characteristics and risk behavior. Blood samples were collected for serological testing of HIV. Of the 402 FSWs, median age and age of initiating sex work were 25 years (Interquartile range [IQR]: 9) and 20 years (IQR: 6), respectively. The majority reported use of alcohol (88.5%), had 5–9 years (median: 9; IQR: 3) of schooling (54.5%), 68.6% had tattoos/body piercings, and 45.1% had more than seven clients per week (median: 7; IQR: 10). Only 32.9% of FSW reported using a condom with nonpaying partners in the last sexual contact. Prevalence of HIV infection was 1.0% (95% CI: 0.1–2.6%). Genotyping for HIV-1 performed on three samples detected subtypes B, C, and F1. Sex work in the Midwestern region of Brazil is characterized by reduced education, large numbers of clients per week, and inconsistent condom use, mainly with nonpaying partners. Although prevalence of HIV infection is currently low, elevated levels of high-risk sexual behavior confirm a need to implement prevention measures. Specific interventions targeting FSWs must emphasize the risk associated with both clients and nonpaying partners while providing knowledge about HIV prevention. Keywords: HIV; female sex workers; sexual behavior; Central Brazil
Introduction Human immunodeficiency virus (HIV) infection represents one of the world’s most serious public health and social issue of growing importance. Joint United Nations Program on HIV/AIDS estimated that there are approximately 34 million people worldwide living with HIV/ AIDS (UNAIDS, 2011). Behavioral risk factors connected to professional activity, such as history of multiple sex partners, inconsistent condom use, and co-infection with other sexually transmitted infections (STIs), make this group of women more vulnerable to HIV infection (Baral et al., 2012; Passos et al., 2007; Wang et al., 2009). Multiple social and structural–environmental factors, such as reduced education, sexual violence, social exclusion, and marginalization of sex work, also play important intersecting roles in stigmatizing female sex workers (FSWs) population (Bautista et al., 2009; Decker et al., 2010; Scorgie et al., 2012). The State of Mato Grosso do Sul (MS) has a highly mobile population as a result of migration from the rural interior and its proximity to border areas with Paraguay *Corresponding author. Email: [email protected] © 2014 Taylor & Francis
and Bolivia, which have high concentrations of population movement and commercial activities, including drug trafficking routes. These conditions may contribute to the spread of HIV in the country (Organization of American States, 1998; Schiray & Fabre, 2002). In order to implement appropriate prevention measures, this study was conducted to describe sociodemographic characteristics and sexual behavior among FSWs in Campo GrandeMS, as well as to determine HIV prevalence and genetic variability among HIV-1 strains.
Methods From November 2009 to December 2011, a survey on the prevalence of HIV among FSWs was conducted in Campo Grande-MS, Brazil. To access hidden populations such as FSWs, respondent-driven sampling (RDS) was chosen as the sampling method. Inclusion criteria for this study were as follows: being a current sex worker (i.e., receiving money or goods in exchange for sexual services), being >18 years old, and self-identifying as female. Transgender sex workers were not included in
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this study. All participants were interviewed using a structured questionnaire and blood samples were collected for HIV screening. All anti-HIV-positive participants were referred to an infectious disease clinic for further clinical assessment and provision of appropriate treatment. The present study was approved by the Research Ethics Committee of the Federal University of Mato Grosso do Sul. Serum samples of participants were initially screened with a commercially enzyme linked immunosorbent assay (ELISA) for detection of antibodies to HIV-1 and HIV-2 (Vironostika HIV Uniform II plus O, Biomérieux). Specimens reactive in ELISA were confirmed by Western blot assay (Novopath HIV-I, Immunoblot, BioRad). Viral RNA was extracted from patient plasma samples using the QIAamp Viral RNA Mini Kit (Qiagen Ltd, Crawley, UK). The HIV-1 protease and reverse transcriptase region were amplified and sequenced using TRUGENE HIV-1 Genotyping Assay and an OpenGene automated DNA software system (Visible Genetics) according to manufacturer’s instructions and data were analyzed as described by Grant et al. (2003). Data were entered into the EPI-INFO 3.4.1 (Center for Diseases Control and Prevention, Atlanta, GA, USA, 1997) statistical software package. The data file was exported and analyzed in Respondent-Driven Sampling Analysis Tool (RDSAT) 5.6.0. RDSAT was used to adjust for differences in network size and for homophily in order to provide population-based estimates of the study population characteristics. Adjusted frequency distributions were calculated along with 95% confidence intervals (CI).
Results A total of 402 FSWs were included as participants in this study. Participant age ranged from 18 to 59 years (median: 25; interquartile range [IQR]: 9). The majority of the sample were single (77.7%), were residents of Campo Grande-MS (93.0%), and had 5–9 years (54.5%; median: 9; IQR: 3) of schooling (Table 1). The characteristics of sex work and risk behavior among FSWs are shown in Table 2. Participation varied by sex work venue, with the greatest participation (83.5%) of FSWs working in massage parlors, show house, and nightclubs, followed by FSWs working at street/bus stations and bars (17.5%). The extent of number of clients attended in the week preceding the interview varied greatly and ranged from 0 to 85 clients, with approximately 45.1% of participants reporting more than seven clients per week (median: 7; IQR: 10). Median age of sexual debut and sex work initiation were 15 years (IQR: 2 years) and 20 years (IQR: 6 years), respectively,
Table 1. Sociodemographic characteristics among FSWs in Campo Grande, Central Brazil, 2009–2011. RDS Variables Age (years) < 21 21–25 26–30 31–35 36–59 Education (years) ≤4 5–9 10–12 >12 Marital status Single Married Separated/ divorced/ widowed Race Mixed White Black Other
Tested, n
Adjusted estimate by RDSAT (%)
CI (95%)
62 143 91 57 49
18.9 40.6 18.2 13.7 8.5
13.1–24.2 33.8–48.1 12.7–23.6 8.8–18.8 5.4–13.7
22 192 175 13
4.2 54.5 39.0 2.3
1.9–7.0 47.5–61.6 31.7–46.3 0.9–4.1
315 52 35
77.7 13.8 8.5
71.1–83.7 9.2–19.1 4.7–12.9
225 129 45 3
57.9 30.0 10.8 1.3
51.2–64.9 23.9–37.1 6.6–14.7 0.1–3.2
with 14.8% engaging in sex work prior to age 18. The proportion of inconsistent condom use with nonpaying partners in the last sexual contact was 67.1%. The presence of vaginal discharge and episode of genital ulcer in the last 12 months was reported by 49.6% and 5.2% of sex workers, respectively. Daily alcohol consumption was reported by 44.2% of FSWs. Approximately 36% of the subjects reported use of illegal drugs. Use of inhaled cocaine and marijuana smoking were frequently reported (90.6%) among drug-using participants, followed by crack (8.3%) and other illegal drugs (5.1%). Only five FSWs reported illicit injection drug use. The overall seroprevalence of anti-HIV in the screened population was 1.0% (6/402; 95% CI: 0.1– 2.6%). The distribution of FSWs’ network according to HIV seroprevalence is shown in Figure 1. Amplified genetic material was only able to be obtained for three samples. HIV-1 subtypes B, C, and F1 were found in these samples. Mutations conferring resistance to nucleosides and nonnucleoside analogs were detected in two samples. In one of these samples which belonged to a participant who was not using antiretroviral drug therapy, the transmission of HIV-1 variants with resistanceassociated mutations was observed.
AIDS Care Table 2. Characteristics of sex work and risk behavior among FSWs in Campo Grande, Central Brazil, 2009–2011.
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Table 2. (Continued) RDS
RDS
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Variables
Tested, n
Adjusted estimate by RDSAT (%)
Variables CI (95%)
Workplace location Massage 141 29.3 13.8–45.7 parlors Show house 130 36.7 22.0–53.1 Nightclubs 60 14.3 8.5–21.0 Street/bus 40 8.7 3.7–12.8 station Bars 37 8.8 2.6–15.2 Closed house 3 1.2 0.3–2.8 Hair/beauty 3 1.0 0.0–3.2 salon Other 5 1.0 0.1–2.4 Charge per client in the last day of work (US$) 5–27 27 7.8 4.0–12.4 28–55 78 24.4 17.0–31.1 56–110 129 34.2 27.5–41.5 111–1444 157 33.6 26.7–41.7 Age at first sex (years) 4–14 152 37.3 30.7–44.2 15–17 200 51.2 44.3–58.1 ≥ 18 49 11.5 7.6–15.8 Ages of sex work initiation (years) < 18 69 14.8 10.2–20.1 ≥ 18 331 85.2 79.9–89.8 Number of clients per week ≤7 203 54.9 47.2–62.0 >7 192 45.1 38.0–52.8 Condom use with clients in last month Always 353 87.7 82.2–92.5 Often 31 6.9 3.8–10.5 Sometimes 13 4.2 1.1–8.1 Never 3 1.2 0.1–3.7 Condom use with intimate and other nonpaying partners in the last sexual contact No 272 67.1 60.2–73.8 Yes 130 32.9 26.2–39.8 Type of sexual intercourse Oral and 185 46.1 41.1–50.9 vaginal Vaginal 147 36.6 31.9–41.3 Anal 2 0.5 0.3–0.7 All 68 17.0 13.3–20.6 Vaginal discharge in the last 12 month No 213 50.4 43.8–56.9 Yes 189 49.6 43.1–56.2 Episode of genital ulcer in the last 12 month No 383 94.8 90.9–97.8 Yes 19 5.2 2.2–9.1 Use of illegal drugs No 233 64.3 57.4–70.9 Yes 169 35.7 29.1–42.6
Tested, n
Tattoo and/or body piercing No 125 Yes 277 Alcohol consumption No 45 All day 215 At least once 125 a week At least once a 17 month
Adjusted estimate by RDSAT (%)
CI (95%)
31.4 68.6
25.0–38.2 61.8–75.1
11.7 44.2 36.2
7.8–16.2 36.8–51.9 29.2–43.1
7.9
3.7–12.7
Discussion This research presented here is the first epidemiological and molecular study of HIV infection in FSWs in the State of Mato Grosso do Sul. In this study, massage parlors, show house, nightclubs, and others closed houses were reported as the main work places for FSWs. Higher rates of HIV prevalence were found among street–based FSWs when compared with FSWs working in nightclubs (Morell, Lacerda, Silva, & Araújo, 2006; Wang et al., 2009), suggesting that street-based FSW are particularly at high risk for transmitting and being infected with HIV due to low access to prevention materials and health care. Many FSWs reported a large number of partners for sexual relations and symptoms suggestive of STI over the previous year (genital ulcer and vaginal discharge). Even taking into account the limitation of this variable in predicting these infections, this finding suggested the potential risk of acquiring HIV infection from FSWs. Indeed, the FSWs studied reported inconsistent condom use, mainly with their nonpaying partners, thereby creating opportunities for spreading STI to the general population. These results highlight the vulnerability of FSWs to both acquisition and transmission of HIV/STIs within complex sexual networks. In our study, a substantial proportion of FSWs (35.7%) reported use of illegal drugs. However, a higher percentage was expected due to the direct relationship between the consumption of illicit drugs with the practice of prostitution, since FSWs work in exchange for drugs or to get money for drugs (Bautista et al., 2009). Injection drug use was fairly rare in this group, suggesting that this risk factor may be a lesser contributor to the spread of HIV in this population. The consumption of alcohol reported among the participants
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Figure 1. Female sex workers’ network according to HIV seroprevalence in Campo Grande-MS, Brazil, 2009–2011.
was high and reasons for drinking varied widely by individual. The concomitant use of alcohol during sexual encounters has serious negative consequences, including unprotected sex (Wang, Li, Stanton, Zhang, & Fang, 2010). The prevalence of HIV infection detected in this study was relatively lower (1.0%) and most likely due to the consistent condom use with clients, lower risk venues as the main place of work and nonuse of injection drugs reported by participants. This low prevalence rate was similar to that found among FSWs (1.2%) across major cities in South America presenting the same characteristics (Bautista et al., 2006) and much lower than those reported in a study conducted among FSWs in 10 Brazilian state capitals (Szwarcwald, de Souza Júnior, Damacena, Junior, & Kendall, 2011) and among streetbased FSWs in different countries (Allen et al., 2006; Nguyen et al., 2004). In Brazil, the HIV-1 subtypes B, F, and C coexist in high-risk groups and the prevalence may differ across geographical regions (Bello, Guimarães, & Morgado, 2006; Schuelter-Trevisol, da Silva, Oliveira, & Rodrigues, 2007). HIV-1 subtypes B, C, and F1 were found in the present study. The circulation of a viral genome associated with drug resistance observed in one sample may represent a serious public health problem and may compromise the Brazilian AIDS program efforts in controlling the dissemination of HIV and antiretroviral therapy management. Like most RDS research, this study was subject to possible methodological limitations regarding data collection and data analysis. First, face-to-face interviews,
such as those conducted here, may have provoked bias involving recall and barriers concerning confidentiality and/or intimate revelations. Despite these limitations, our findings have important implications for future research and prevention efforts targeting these populations in Brazil. In summary, low prevalence of HIV infection was observed among FSWs in Campo Grande-MS, Brazil. However, the presence of different sexual risk behaviors among this vulnerable and hard-to-reach population confirms the need for additional health education and prevention programs focusing not only on the high risks associated with clients but also the risks with nonpaying partners. Acknowledgments The authors acknowledge all the FSWs who participated in this study and the important contribution of members of nongovernmental organizations (NGOs).
Funding This work was supported by Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul [FUNDECT/MS/CNPq/SES n° 07/2009]; Conselho Nacional de Desenvolvimento Científico e Tecnológico [MCT/CNPq/SPM-PR/MDA n°57/2008].
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AIDS Care Deficiency Syndromes, 43, 96–101. doi:10.1097/01. qai.0000226794.23840.80 Baral, S., Beyrer, C., Muessig, K., Poteat, T., Wirts, A. L., Decker, M. R., … Kerrigan, D. (2012). Burden of HIV among female sex workers in low-income and middleincome countries: A systematic review and meta-analysis. The Lancet Infectious Diseases, 12, 538–549. doi:10.1016/ S1473-3099(12)70066-X Bautista, C. T., Sanchez, J. L., Montano, S. M., Laguna-Torres, A., Suarez, L., Sanchez, J., … Carr, J. J. (2006). Seroprevalence of and risk factors for HIV-1 infection among female commercial sex workers in South America. Sexually Transmitted Infections, 82, 311–316. doi:10. 1136/sti.2005.018234 Bautista, C. T., Pando, M. A., Reynaga, E., Marone, R., Sateren, W. B., Montano, S. M., … Avila, M. M. (2009). Sexual practices, drug use behaviors, and prevalence of HIV, syphilis, hepatitis B and C, and HTLV-1/2 in immigrant and non-immigrant female sex workers in Argentina. Journal of Immigrant and Minority Health, 11, 99–104. doi:10.1007/s10903-007-9114-2 Bello, G., Guimarães, M. L., & Morgado, M. G. (2006). Evolutionary history of HIV-1 subtype B and F infections in Brazil. AIDS, 20, 763–768. doi:10.1097/01.aids.0000 216377.84313.52 Decker, M. R., McCauley, H. L., Phuengsamran, D., Janyam, S., Seage, G. R., & Silverman, J. G. (2010). Violence victimisation, sexual risk and sexually transmitted infection symptoms among female sex workers in Thailand. Sexually Transmitted Infections, 86, 236–240. doi:10.11 36/sti.2009.037846 Grant, R. M., Kuritzkes, D. R., Johnson, V. A., Mellors, J. W., Sullivan, J. L., Swanstrom, R., … Winslow, D. L. (2003). Accuracy of the TRUGENE HIV-1 genotyping kit. Journal of Clinical Microbiology, 41, 1586–1593. doi:10.1128/JCM.41.4.1586-1593.2003 Morell, M. G. G., Lacerda, R. M., Silva, N. G., & Araújo, N. (2006). Respondent driven sampling (RDS): An effective methodology to estimate HIV transmission vulnerability among sex workers from Santos. In Research report Brazilian National STD/AIDS Program. Brasília: Brazilian Ministry of Health. Nguyen, A. T., Nguyen, T. H., Pham, K. C., Le, T. G., Bui, D. T., Hoang, T. L., … Detels, R. (2004). Intravenous drug use among street-based sex workers: A high-risk behavior for HIV transmission. Sexually Transmitted Diseases, 31, 15–19. doi:10.1097/01.OLQ.0000105002.34902.B5
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AIDS Care: Psychological and Socio-medical Aspects of AIDS/HIV Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/caic20
HIV seroprevalence and high-risk sexual behavior among female sex workers in Central Brazil a
a
a
a
Fernanda R.P. Fernandes , Gina J. Mousquer , Lisie S. Castro , Marco A. Puga , Tayana S.O. a
a
a
a
b
Tanaka , Grazielli R. Rezende , Clarice S. Pinto , Larissa M. Bandeira , Regina M.B. Martins , c
d
Roberta B.L. Francisco , Sheila A. Teles & Ana R.C. Motta-Castro
a
a
Department of Biochemistry and Pharmacy, Federal University of Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil b
Institute of Tropical Pathology and Public Health, Federal University of Goiás, Goiânia, Brazil
Click for updates
c
Central Public Health Laboratory, LACEN/MS, Campo Grande, Brazil
d
School of Nursing, Federal University of Goias, Goiânia, Brazil Published online: 12 Mar 2014.
To cite this article: Fernanda R.P. Fernandes, Gina J. Mousquer, Lisie S. Castro, Marco A. Puga, Tayana S.O. Tanaka, Grazielli R. Rezende, Clarice S. Pinto, Larissa M. Bandeira, Regina M.B. Martins, Roberta B.L. Francisco, Sheila A. Teles & Ana R.C. Motta-Castro (2014) HIV seroprevalence and high-risk sexual behavior among female sex workers in Central Brazil, AIDS Care: Psychological and Socio-medical Aspects of AIDS/HIV, 26:9, 1095-1099, DOI: 10.1080/09540121.2014.894609 To link to this article: http://dx.doi.org/10.1080/09540121.2014.894609
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
AIDS Care, 2014 Vol. 26, No. 9, 1095–1099, http://dx.doi.org/10.1080/09540121.2014.894609
HIV seroprevalence and high-risk sexual behavior among female sex workers in Central Brazil Fernanda R.P. Fernandesa*, Gina J. Mousquera, Lisie S. Castroa, Marco A. Pugaa, Tayana S.O. Tanakaa, Grazielli R. Rezendea, Clarice S. Pintoa, Larissa M. Bandeiraa, Regina M.B. Martinsb, Roberta B.L. Franciscoc, Sheila A. Telesd and Ana R.C. Motta-Castroa a
Department of Biochemistry and Pharmacy, Federal University of Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil; Institute of Tropical Pathology and Public Health, Federal University of Goiás, Goiânia, Brazil; cCentral Public Health Laboratory, LACEN/MS, Campo Grande, Brazil; dSchool of Nursing, Federal University of Goias, Goiânia, Brazil b
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(Received 9 May 2013; accepted 11 February 2014) Female sex workers (FSWs) are considered a high-risk group for human immunodeficiency virus (HIV) infection due to their social vulnerability and factors associated with their work. We estimated the prevalence of HIV, and identified viral subtypes and risk factors among FSWs. A cross-sectional study using respondent-driven sampling (RDS) method was conducted among 402 FSWs in Campo Grande city, Brazil, from 2009 to 2011. Participants were interviewed using a standardized questionnaire about sociodemograpic characteristics and risk behavior. Blood samples were collected for serological testing of HIV. Of the 402 FSWs, median age and age of initiating sex work were 25 years (Interquartile range [IQR]: 9) and 20 years (IQR: 6), respectively. The majority reported use of alcohol (88.5%), had 5–9 years (median: 9; IQR: 3) of schooling (54.5%), 68.6% had tattoos/body piercings, and 45.1% had more than seven clients per week (median: 7; IQR: 10). Only 32.9% of FSW reported using a condom with nonpaying partners in the last sexual contact. Prevalence of HIV infection was 1.0% (95% CI: 0.1–2.6%). Genotyping for HIV-1 performed on three samples detected subtypes B, C, and F1. Sex work in the Midwestern region of Brazil is characterized by reduced education, large numbers of clients per week, and inconsistent condom use, mainly with nonpaying partners. Although prevalence of HIV infection is currently low, elevated levels of high-risk sexual behavior confirm a need to implement prevention measures. Specific interventions targeting FSWs must emphasize the risk associated with both clients and nonpaying partners while providing knowledge about HIV prevention. Keywords: HIV; female sex workers; sexual behavior; Central Brazil
Introduction Human immunodeficiency virus (HIV) infection represents one of the world’s most serious public health and social issue of growing importance. Joint United Nations Program on HIV/AIDS estimated that there are approximately 34 million people worldwide living with HIV/ AIDS (UNAIDS, 2011). Behavioral risk factors connected to professional activity, such as history of multiple sex partners, inconsistent condom use, and co-infection with other sexually transmitted infections (STIs), make this group of women more vulnerable to HIV infection (Baral et al., 2012; Passos et al., 2007; Wang et al., 2009). Multiple social and structural–environmental factors, such as reduced education, sexual violence, social exclusion, and marginalization of sex work, also play important intersecting roles in stigmatizing female sex workers (FSWs) population (Bautista et al., 2009; Decker et al., 2010; Scorgie et al., 2012). The State of Mato Grosso do Sul (MS) has a highly mobile population as a result of migration from the rural interior and its proximity to border areas with Paraguay *Corresponding author. Email: [email protected] © 2014 Taylor & Francis
and Bolivia, which have high concentrations of population movement and commercial activities, including drug trafficking routes. These conditions may contribute to the spread of HIV in the country (Organization of American States, 1998; Schiray & Fabre, 2002). In order to implement appropriate prevention measures, this study was conducted to describe sociodemographic characteristics and sexual behavior among FSWs in Campo GrandeMS, as well as to determine HIV prevalence and genetic variability among HIV-1 strains.
Methods From November 2009 to December 2011, a survey on the prevalence of HIV among FSWs was conducted in Campo Grande-MS, Brazil. To access hidden populations such as FSWs, respondent-driven sampling (RDS) was chosen as the sampling method. Inclusion criteria for this study were as follows: being a current sex worker (i.e., receiving money or goods in exchange for sexual services), being >18 years old, and self-identifying as female. Transgender sex workers were not included in
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this study. All participants were interviewed using a structured questionnaire and blood samples were collected for HIV screening. All anti-HIV-positive participants were referred to an infectious disease clinic for further clinical assessment and provision of appropriate treatment. The present study was approved by the Research Ethics Committee of the Federal University of Mato Grosso do Sul. Serum samples of participants were initially screened with a commercially enzyme linked immunosorbent assay (ELISA) for detection of antibodies to HIV-1 and HIV-2 (Vironostika HIV Uniform II plus O, Biomérieux). Specimens reactive in ELISA were confirmed by Western blot assay (Novopath HIV-I, Immunoblot, BioRad). Viral RNA was extracted from patient plasma samples using the QIAamp Viral RNA Mini Kit (Qiagen Ltd, Crawley, UK). The HIV-1 protease and reverse transcriptase region were amplified and sequenced using TRUGENE HIV-1 Genotyping Assay and an OpenGene automated DNA software system (Visible Genetics) according to manufacturer’s instructions and data were analyzed as described by Grant et al. (2003). Data were entered into the EPI-INFO 3.4.1 (Center for Diseases Control and Prevention, Atlanta, GA, USA, 1997) statistical software package. The data file was exported and analyzed in Respondent-Driven Sampling Analysis Tool (RDSAT) 5.6.0. RDSAT was used to adjust for differences in network size and for homophily in order to provide population-based estimates of the study population characteristics. Adjusted frequency distributions were calculated along with 95% confidence intervals (CI).
Results A total of 402 FSWs were included as participants in this study. Participant age ranged from 18 to 59 years (median: 25; interquartile range [IQR]: 9). The majority of the sample were single (77.7%), were residents of Campo Grande-MS (93.0%), and had 5–9 years (54.5%; median: 9; IQR: 3) of schooling (Table 1). The characteristics of sex work and risk behavior among FSWs are shown in Table 2. Participation varied by sex work venue, with the greatest participation (83.5%) of FSWs working in massage parlors, show house, and nightclubs, followed by FSWs working at street/bus stations and bars (17.5%). The extent of number of clients attended in the week preceding the interview varied greatly and ranged from 0 to 85 clients, with approximately 45.1% of participants reporting more than seven clients per week (median: 7; IQR: 10). Median age of sexual debut and sex work initiation were 15 years (IQR: 2 years) and 20 years (IQR: 6 years), respectively,
Table 1. Sociodemographic characteristics among FSWs in Campo Grande, Central Brazil, 2009–2011. RDS Variables Age (years) < 21 21–25 26–30 31–35 36–59 Education (years) ≤4 5–9 10–12 >12 Marital status Single Married Separated/ divorced/ widowed Race Mixed White Black Other
Tested, n
Adjusted estimate by RDSAT (%)
CI (95%)
62 143 91 57 49
18.9 40.6 18.2 13.7 8.5
13.1–24.2 33.8–48.1 12.7–23.6 8.8–18.8 5.4–13.7
22 192 175 13
4.2 54.5 39.0 2.3
1.9–7.0 47.5–61.6 31.7–46.3 0.9–4.1
315 52 35
77.7 13.8 8.5
71.1–83.7 9.2–19.1 4.7–12.9
225 129 45 3
57.9 30.0 10.8 1.3
51.2–64.9 23.9–37.1 6.6–14.7 0.1–3.2
with 14.8% engaging in sex work prior to age 18. The proportion of inconsistent condom use with nonpaying partners in the last sexual contact was 67.1%. The presence of vaginal discharge and episode of genital ulcer in the last 12 months was reported by 49.6% and 5.2% of sex workers, respectively. Daily alcohol consumption was reported by 44.2% of FSWs. Approximately 36% of the subjects reported use of illegal drugs. Use of inhaled cocaine and marijuana smoking were frequently reported (90.6%) among drug-using participants, followed by crack (8.3%) and other illegal drugs (5.1%). Only five FSWs reported illicit injection drug use. The overall seroprevalence of anti-HIV in the screened population was 1.0% (6/402; 95% CI: 0.1– 2.6%). The distribution of FSWs’ network according to HIV seroprevalence is shown in Figure 1. Amplified genetic material was only able to be obtained for three samples. HIV-1 subtypes B, C, and F1 were found in these samples. Mutations conferring resistance to nucleosides and nonnucleoside analogs were detected in two samples. In one of these samples which belonged to a participant who was not using antiretroviral drug therapy, the transmission of HIV-1 variants with resistanceassociated mutations was observed.
AIDS Care Table 2. Characteristics of sex work and risk behavior among FSWs in Campo Grande, Central Brazil, 2009–2011.
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Table 2. (Continued) RDS
RDS
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Variables
Tested, n
Adjusted estimate by RDSAT (%)
Variables CI (95%)
Workplace location Massage 141 29.3 13.8–45.7 parlors Show house 130 36.7 22.0–53.1 Nightclubs 60 14.3 8.5–21.0 Street/bus 40 8.7 3.7–12.8 station Bars 37 8.8 2.6–15.2 Closed house 3 1.2 0.3–2.8 Hair/beauty 3 1.0 0.0–3.2 salon Other 5 1.0 0.1–2.4 Charge per client in the last day of work (US$) 5–27 27 7.8 4.0–12.4 28–55 78 24.4 17.0–31.1 56–110 129 34.2 27.5–41.5 111–1444 157 33.6 26.7–41.7 Age at first sex (years) 4–14 152 37.3 30.7–44.2 15–17 200 51.2 44.3–58.1 ≥ 18 49 11.5 7.6–15.8 Ages of sex work initiation (years) < 18 69 14.8 10.2–20.1 ≥ 18 331 85.2 79.9–89.8 Number of clients per week ≤7 203 54.9 47.2–62.0 >7 192 45.1 38.0–52.8 Condom use with clients in last month Always 353 87.7 82.2–92.5 Often 31 6.9 3.8–10.5 Sometimes 13 4.2 1.1–8.1 Never 3 1.2 0.1–3.7 Condom use with intimate and other nonpaying partners in the last sexual contact No 272 67.1 60.2–73.8 Yes 130 32.9 26.2–39.8 Type of sexual intercourse Oral and 185 46.1 41.1–50.9 vaginal Vaginal 147 36.6 31.9–41.3 Anal 2 0.5 0.3–0.7 All 68 17.0 13.3–20.6 Vaginal discharge in the last 12 month No 213 50.4 43.8–56.9 Yes 189 49.6 43.1–56.2 Episode of genital ulcer in the last 12 month No 383 94.8 90.9–97.8 Yes 19 5.2 2.2–9.1 Use of illegal drugs No 233 64.3 57.4–70.9 Yes 169 35.7 29.1–42.6
Tested, n
Tattoo and/or body piercing No 125 Yes 277 Alcohol consumption No 45 All day 215 At least once 125 a week At least once a 17 month
Adjusted estimate by RDSAT (%)
CI (95%)
31.4 68.6
25.0–38.2 61.8–75.1
11.7 44.2 36.2
7.8–16.2 36.8–51.9 29.2–43.1
7.9
3.7–12.7
Discussion This research presented here is the first epidemiological and molecular study of HIV infection in FSWs in the State of Mato Grosso do Sul. In this study, massage parlors, show house, nightclubs, and others closed houses were reported as the main work places for FSWs. Higher rates of HIV prevalence were found among street–based FSWs when compared with FSWs working in nightclubs (Morell, Lacerda, Silva, & Araújo, 2006; Wang et al., 2009), suggesting that street-based FSW are particularly at high risk for transmitting and being infected with HIV due to low access to prevention materials and health care. Many FSWs reported a large number of partners for sexual relations and symptoms suggestive of STI over the previous year (genital ulcer and vaginal discharge). Even taking into account the limitation of this variable in predicting these infections, this finding suggested the potential risk of acquiring HIV infection from FSWs. Indeed, the FSWs studied reported inconsistent condom use, mainly with their nonpaying partners, thereby creating opportunities for spreading STI to the general population. These results highlight the vulnerability of FSWs to both acquisition and transmission of HIV/STIs within complex sexual networks. In our study, a substantial proportion of FSWs (35.7%) reported use of illegal drugs. However, a higher percentage was expected due to the direct relationship between the consumption of illicit drugs with the practice of prostitution, since FSWs work in exchange for drugs or to get money for drugs (Bautista et al., 2009). Injection drug use was fairly rare in this group, suggesting that this risk factor may be a lesser contributor to the spread of HIV in this population. The consumption of alcohol reported among the participants
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Figure 1. Female sex workers’ network according to HIV seroprevalence in Campo Grande-MS, Brazil, 2009–2011.
was high and reasons for drinking varied widely by individual. The concomitant use of alcohol during sexual encounters has serious negative consequences, including unprotected sex (Wang, Li, Stanton, Zhang, & Fang, 2010). The prevalence of HIV infection detected in this study was relatively lower (1.0%) and most likely due to the consistent condom use with clients, lower risk venues as the main place of work and nonuse of injection drugs reported by participants. This low prevalence rate was similar to that found among FSWs (1.2%) across major cities in South America presenting the same characteristics (Bautista et al., 2006) and much lower than those reported in a study conducted among FSWs in 10 Brazilian state capitals (Szwarcwald, de Souza Júnior, Damacena, Junior, & Kendall, 2011) and among streetbased FSWs in different countries (Allen et al., 2006; Nguyen et al., 2004). In Brazil, the HIV-1 subtypes B, F, and C coexist in high-risk groups and the prevalence may differ across geographical regions (Bello, Guimarães, & Morgado, 2006; Schuelter-Trevisol, da Silva, Oliveira, & Rodrigues, 2007). HIV-1 subtypes B, C, and F1 were found in the present study. The circulation of a viral genome associated with drug resistance observed in one sample may represent a serious public health problem and may compromise the Brazilian AIDS program efforts in controlling the dissemination of HIV and antiretroviral therapy management. Like most RDS research, this study was subject to possible methodological limitations regarding data collection and data analysis. First, face-to-face interviews,
such as those conducted here, may have provoked bias involving recall and barriers concerning confidentiality and/or intimate revelations. Despite these limitations, our findings have important implications for future research and prevention efforts targeting these populations in Brazil. In summary, low prevalence of HIV infection was observed among FSWs in Campo Grande-MS, Brazil. However, the presence of different sexual risk behaviors among this vulnerable and hard-to-reach population confirms the need for additional health education and prevention programs focusing not only on the high risks associated with clients but also the risks with nonpaying partners. Acknowledgments The authors acknowledge all the FSWs who participated in this study and the important contribution of members of nongovernmental organizations (NGOs).
Funding This work was supported by Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul [FUNDECT/MS/CNPq/SES n° 07/2009]; Conselho Nacional de Desenvolvimento Científico e Tecnológico [MCT/CNPq/SPM-PR/MDA n°57/2008].
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