HIV risk practices by female sex workers according to workplace

Giseli Nogueira Damacena Célia Landmann Szwarcwald Paulo Roberto Borges de Souza Júnior

Abstracts

OBJECTIVE

To investigate differences in HIV infection- related risk practices by Female Sex Workers according to workplace and the effects of homophily on estimating HIV prevalence.

METHODS

Data from 2,523 women, recruited using Respondent-Driven Sampling, were used for the study carried out in 10 Brazilian cities in 2008-2009. The study included female sex workers aged 18 and over. The questionnaire was completed by the subjects and included questions on characteristics of professional activity, sexual practices, use of drugs, HIV testing, and access to health services. HIV quick tests were conducted. The participants were classified in two groups according to place of work: on the street or indoor venues, like nightclubs and saunas. To compare variable distributions by place of work, we used Chi-square homogeneity tests, taking into consideration unequal selection probabilities as well as the structure of dependence between observations. We tested the effect of homophily by workplace on estimated HIV prevalence.

RESULTS

The highest HIV risk practices were associated with: working on the streets, lower socioeconomic status, low regular smear test coverage, higher levels of crack use and higher levels of syphilis serological scars as well as higher prevalence of HIV infection. The effect of homophily was higher among sex workers in indoor venues. However, it did not affect the estimated prevalence of HIV, even after using a post-stratification by workplace procedure.

CONCLUSIONS

The findings suggest that strategies should focus on extending access to, and utilization of, health services. Prevention policies should be specifically aimed at street workers. Regarding the application of Respondent-Driven Sampling, the sample should be sufficient to estimate transition probabilities, as the network develops more quickly among sex workers in indoor venues.

Sex Workers; Dangerous Behavior; HIV Seroprevalence; Risk Factors; Workplace


INTRODUCTION

It is necessary to monitor the practices and attitudes of those most at risk of HIV infection, as specific interventions aimed at these population subgroups can significantly alter the pattern of the spread of HIV and AIDS in the general population.5 Boily MC, Lowdes C, Alary M. The impact of HIV epidemic phases on the effectiveness of core group interventions: insights from mathematical models. Sex Transm Infect. 2002;78(Suppl 1):78-90. DOI:10.1136/sti.78.suppl_1.i78

Research on female sex workers (FSW) confirms the increased risk of HIV infection in this population subgroup. Lack of access to health care services, drug abuse and prior history of sexually transmitted infection have also been shown, and are also factors associated with HIV prevalence.2020  Li J, Chen XS, Merli MG, Weir SS, Henderson GR. Systematic differences in risk behaviors and syphilis prevalence across types of female sex workers: a preliminary study in Liuzhou, China. Sex Transm Dis. 2012;39(3):195-200. DOI:10.1097/OLQ.0b013e31823d2e2a,2323  Medhi GK, Mahanta J, Kermode M, Paranjape RS, Adhikary R, Phukan SK, et al. Factors associated with history of drug use among female sex workers (FSW) in a high HIV prevalence state of India. BMC Public Health. 2012;12:273. DOI:10.1186/1471-2458-12-273 Recent studies emphasize the importance of characterizing FSW practice according to workplace. Practices placing them at risk of HIV infection may vary according to where the FSW meet their clients (indoor venues or on the street).4 Blankenship KM, Burroway R, Reed E. Factors associated with awareness and utilisation of a community mobilisation intervention for female sex workers in Andhra Pradesh, India. Sex Transm Infect. 2010;86(Suppl 1):69-75.,7 Buzdugan R, Copas A, Moses S, Blanchard J, Isac S, Ramesh BM, et al. Devising a female sex work typology using data from Karnataka, India. Int J Epidemiol. 2010;39(2):439-48. DOI:10.1093/ije/dyp351,2020  Li J, Chen XS, Merli MG, Weir SS, Henderson GR. Systematic differences in risk behaviors and syphilis prevalence across types of female sex workers: a preliminary study in Liuzhou, China. Sex Transm Dis. 2012;39(3):195-200. DOI:10.1097/OLQ.0b013e31823d2e2a,2121  Li Y, Detels R, Lin P, Fu X, Deng Z, Liu Y, et al. Difference in risk behaviors and STD prevalence between street-based and establishment-based FSWs in Guangdong Province, China. AIDS Behav. 2012;16(4):943-51. DOI:10.1007/s10461-011-0102-0

Until recently, convenience sampling was used in studies of this type, due to the difficulties in using traditional sampling techniques to select individuals in populations with high risk of HIV infection.2525  Pascom AR, Szwarcwald CL, Barbosa-Jr A. Sampling studies to estimate the HIV prevalence rate in female commercial sex workers. Braz J Infect Dis. 2010;14(4):385-97. DOI:10.1590/S1413-86702010000400014 These studies were also local, limiting monitoring of national level prevention actions and policies.3 Barbosa-Jr A, Pascom ARP, Szwarcwald CL, Kendall C, McFarland W. Transfer of sampling methods for studies on most-at-risk populations (MARPs) in Brazil. Cad Saude Publica. 2011;27(Suppl 1):36-44. DOI:10.1590/S0102-311X2011001300005 

The development of probabilistic sampling methods specifically for selecting individuals at greater risk of contracting HIV, such as Respondent-Driven Sampling (RDS),1414  Heckathorn DD. Respondent-driven sampling: a new approach to the study of hidden populations. Soc Probl. 1997;4492:174-99. DOI:10.2307/3096941 gave new opportunities for both international2222  Malekinejad M, Johnston LG, Kendall C, Kerr LR, Rifkin MR, Rutherford GW. Using respondentdriven sampling methodology for HIV biological and behavioral surveillance in international settings: a systematic review. AIDS Behav. 2008;12(4Suppl):105-30. DOI:10.1007/s10461-008-9421-1 and national research.1717  Kerr LR, Mota RS, Kendall C, Pinho AA, Mello MB, Guimarães MD, et al. HIV among MSM in a large middle-income country. AIDS. 2013;27(3):427-35. DOI:10.1097/QAD.0b013e32835ad504

RDS is considered to be a variant of chain sampling. However, it was developed based on assumptions that allow the probability of selection to be calculated.2626  Salganik MJ, Heckathorn DD. Sampling and estimation in hidden populations using Respondent-Driven Sampling. Sociol Methodol. 2004;3491:193-240. DOI:10.1111/j.0081-1750.2004.00152.x Recruiting individuals using RDS assumes that individuals with a certain characteristic or participating in a certain activity are interlinked through a social network and have connections with others with similar characteristics. The data are collected in successive recruitment circles, known as “waves”.1414  Heckathorn DD. Respondent-driven sampling: a new approach to the study of hidden populations. Soc Probl. 1997;4492:174-99. DOI:10.2307/3096941 The method sometimes produces the so-called “homophily effect”, a result of the tendency of the individual selected for the study to recruit others with similar charateristics.1515  Heckathorn DD, Semaan S, Broadhead RS, Hughes JJ. Extensions of respondent-driven sampling: a new approach to the study of injection drug users aged 18-25. AIDS Behav. 2002;6(1):55-67. DOI:10.1023/A:1014528612685

In 2008 and 2009, a study with FSW was conducted in 10 cities in Brazil, with RDS chosen as the sampling methodology.1010  Damacena GN, Szwarcwald CL, Barbosa Jr A. Implementation of respondent-driven sampling among female sex workers in Brazil, 2009. Cad Saude Publica. 2011;27(Suppl 1):S45-55. DOI:10.1590/S0102-311X2011001300006,1111  Damacena GN, Szwarcwald CL, Souza-Jr PRB, Dourado I. Risk factors associated with HIV prevalence among female sex workers in 10 Brazilian cities. J Acquir Immune Defic Syndr. 2011;57(Suppl 3):144-52. DOI:10.1097/QAI.0b013e31821e9bf6,2828  Szwarcwald CL, Souza-Jr PRB, Damacena GN, Barbosa-Jr A, Kendall C. Analysis of data collected by RDS among sex workers in 10 Brazilian cities, 2009: estimation of the prevalence of HIV, variance, and design effect. J Acquir Immune Defic Syndr. 2011;57(Suppl 3):129-35 DOI:10.1097/QAI.0b013e31821e9a36 Based on the data from this study, Szwarcwald et al2828  Szwarcwald CL, Souza-Jr PRB, Damacena GN, Barbosa-Jr A, Kendall C. Analysis of data collected by RDS among sex workers in 10 Brazilian cities, 2009: estimation of the prevalence of HIV, variance, and design effect. J Acquir Immune Defic Syndr. 2011;57(Suppl 3):129-35 DOI:10.1097/QAI.0b013e31821e9a36 proposed a method of analyzing data collected using RDS, taking into consideration unequal probability of selection as well as dependency between observations, given the recruitment pattern as well as intraclass variation in the group of participants recruited by the same person. Moreover, the analysis can be conducted using logistic regression, enabling the model to be extended to a multivariate model. The prevalence of HIV was estimated at 4.8% (95%CI 3.4;6.1), approximately 15 times greater in this group than in the female Brazilian population.2727  Szwarcwald CL, Barbosa Jr A, Souza Jr PRB, Lemos KR, Frias PG, Luhm KR, et al. HIV testing during pregnancy: use of secondary data to estimate 2006 test coverage and prevalence in Brazil. Braz J Infect Dis. 2008;12(3):167-172. DOI:10.1590/S1413-86702008000300002 Multivariate analysis showed that the length of time in prostitution, charging low prices, presence of other sexually transmitted infections and the possibility of being pressured by the client not to use protection were the main predictors of HIV in Brazilian FSW.1111  Damacena GN, Szwarcwald CL, Souza-Jr PRB, Dourado I. Risk factors associated with HIV prevalence among female sex workers in 10 Brazilian cities. J Acquir Immune Defic Syndr. 2011;57(Suppl 3):144-52. DOI:10.1097/QAI.0b013e31821e9bf6

This article aimed to investigate differences in HIV infection-related practices in female sex workers according to the workplace, and the effects of homophily in estimating HIV prevalence.

METHODS

Data were taken from the study on sexually transmitted infections in sex workers, which took place between August 2008 and July 2009 in 10 Brazilian cities (Manaus, Recife, Salvador, Campo Grande, Brasília, Belo Horizonte, Santos, Rio de Janeiro, Curitiba and Itajaí).

The cities were chosen by the Brazilian Ministry of Health Department of Sexually Transmitted Diseases, AIDS and Viral Hepatitis due to their location and the scale of the HIV/AIDS epidemic.

In total, 2,523 FSW aged 18 and over, who had had sex in exchange for money on at least one occasion in the four months preceding the study, were included. The sample was proportional to the population of each city, although with a minimum of 100 FSW.1010  Damacena GN, Szwarcwald CL, Barbosa Jr A. Implementation of respondent-driven sampling among female sex workers in Brazil, 2009. Cad Saude Publica. 2011;27(Suppl 1):S45-55. DOI:10.1590/S0102-311X2011001300006

In each city, 10 initial participants, so-called “seeds”, were chosen. The choice of seeds was not random, as it was to include FSW of different ages groups, skin color/race, economic class, level of schooling and from different workplaces, e.g., on the street, in nightclubs, saunas, and hotels, among others. Each seed received three coupons to pass on to acquaintances who were also sex workers. Those seeds invited to participate in the research formed the first “wave” of the study. After participating in an interview they in turn received three more coupons to invite their acquaintances. This process was repeated until the required sample for each city was reached.

The data were collected using a questionnaire in an Audio Computer-Assisted Self-Interview. The FSW were provided with laptop computers and headphones with which to read and listen to all of the questions and response options in private. Studies conducted in the USA indicate that interview methods that increase privacy in the context of the interview dramatically increase reports regarding sensitive and/or illegal behavior.1 Aquilino WS. Privacy effects on self-reported drug use: interactions with survey mode and respondents characteristics. NIDA Res Monogr. 1997;167:383-415.,1818  Kissinger P, Rice J, Farley T, Trim S, Jewitt K, Margavio V, et al. Application of computer-assisted interviews to sexual behavior research. Am J Epidemiol.1999;149(10):950-4. DOI:10.1093/oxfordjournals.aje.a009739 They also indicated that the participants had no difficulty in using the equipment.2424  O’Reilly JM, Hubbard ML, Lessler JT, Biemer PP, Turner CF. Audio and video computer assisted self-interviewing: preliminary tests of new technologies for data collection. J Off Stat. 1994;1092:197-214.,2525  Pascom AR, Szwarcwald CL, Barbosa-Jr A. Sampling studies to estimate the HIV prevalence rate in female commercial sex workers. Braz J Infect Dis. 2010;14(4):385-97. DOI:10.1590/S1413-86702010000400014,aa Rogers SM, Miller HG, Forsyth BH, Smith TK, Turner CF. Audio-CASI: the impact of operational characteristics on data quality. Joint Proceedings of the American Association for Public Opinion Research. 1996; Alexandria; US. Alexandria: American Statistical Association, Survey Methods Research Section; 1996.

HIV diagnosis was obtained using the rapid test, following the protocols of the Department of Sexually Transmitted Diseases, AIDS and Viral Hepatitis. To verify any association with the prevalence of syphilis with that of HIV, the disease was tested for using the Bio-Line rapid treponemal test for syphilis which gave a diagnosis of active syphilis. Negative or positive VDRL tests below 1:8 were considered to be a syphilis serologic scar. All participants received pre- and post-test counselling. Women with positive results received additional post-test counselling, both in order to deal with the psychological impact and to encourage partners to be tested if necessary, and were referred to public health care services for follow up.

The assumptions of the RDS method and the experience of establishing this sampling process in sex workers in Brazil are described in a previous publication.1010  Damacena GN, Szwarcwald CL, Barbosa Jr A. Implementation of respondent-driven sampling among female sex workers in Brazil, 2009. Cad Saude Publica. 2011;27(Suppl 1):S45-55. DOI:10.1590/S0102-311X2011001300006

The size of the FSW network of acquaintances was estimated using the question: “How many sex workers working here in the city do you know personally?”, and sampling weights proportional to the inverse of the size of the participants’ network were used.2626  Salganik MJ, Heckathorn DD. Sampling and estimation in hidden populations using Respondent-Driven Sampling. Sociol Methodol. 2004;3491:193-240. DOI:10.1111/j.0081-1750.2004.00152.x The total sample was calibrated using post-stratification procedures, considering the relative size of the group of 18 to 59-year-old women in each city and assuming the same proportion of FSW in all cities.2828  Szwarcwald CL, Souza-Jr PRB, Damacena GN, Barbosa-Jr A, Kendall C. Analysis of data collected by RDS among sex workers in 10 Brazilian cities, 2009: estimation of the prevalence of HIV, variance, and design effect. J Acquir Immune Defic Syndr. 2011;57(Suppl 3):129-35 DOI:10.1097/QAI.0b013e31821e9a36

The FSW were separated into two groups according to their workplace: the “on the street” group composed of those who worked on the street and in brothels; and the “indoor venues” group, made up of women who worked in nightclubs, bars, hotels, motels, saunas and massage parlors.

The following aspects were used to investigate differences according to workplace: sociodemographic variables, characteristics of the FSW work, frequency of alcohol and illegal drug use, health service access indicators and the results of the HIV and syphilis tests. Indicators of condom use were not used as they show no significant association with HIV infection.1111  Damacena GN, Szwarcwald CL, Souza-Jr PRB, Dourado I. Risk factors associated with HIV prevalence among female sex workers in 10 Brazilian cities. J Acquir Immune Defic Syndr. 2011;57(Suppl 3):144-52. DOI:10.1097/QAI.0b013e31821e9bf6

The comparative analysis used the Chi-square tests for homogeneity between distributions, taking into consideration unequal probabilities of selection as well as dependence between observations given the intra-class variation between participants recruited by the same individual. The “Complex Sample” appendix from the Statistical Package for the Social Sciences 17.0 was used, considering the group of women invited by the same FSW as a cluster.

To verify homophily according to workplace, the recruitment network was analyzed identifying the workplace of the recruiter and the recruitee, using the NetDraw program.6 Borgatti SP. NetDraw Software for Network Visualization. Lexington: Analytic Technologies; 2002. Estimates of the proportion of FSW in each stratum and the homophily test were conducted using estimates of the probability of transition from one state (the street) to the other (indoor venue), using the method proposed by Szwarcwald et al.2828  Szwarcwald CL, Souza-Jr PRB, Damacena GN, Barbosa-Jr A, Kendall C. Analysis of data collected by RDS among sex workers in 10 Brazilian cities, 2009: estimation of the prevalence of HIV, variance, and design effect. J Acquir Immune Defic Syndr. 2011;57(Suppl 3):129-35 DOI:10.1097/QAI.0b013e31821e9a36

Additionally, the possible effects of homophily according to workplace in estimating HIV prevalence were also investigated. Considering stratification according to workplace, the estimate of HIV prevalence is found by:

,

In which i = 1 and 2 represent strata and P(HIV| i), the prevalence of HIV in stratum i.

The research was approved by the Research Ethics Committee of the Fundação Oswaldo Cruz (Protocol 395/07).

RESULTS

There were 2,523 interviews, excluding those of the seeds, distributed among the 10 cities: Manaus (199), Recife (237), Salvador (260), Campo Grande (147), Brasília (308), Belo Horizonte (289), Santos (191), Rio de Janeiro (601), Curitiba (201) and Itajaí (90).

When comparing the sociodemographic characteristics of the FSW according to workplace, with the exception of race, all the variables studied showed statistically significant differences at the 5% level. Comparing distributions according to age, the majority of young women (18 to 24 years old) were found in the “indoor venue” group, whereas the majority of FSW aged 40 and over were in the “on the street” group. In regard to socioeconomic status, FSW in indoor venues had higher levels of schooling and income above R$ 1,200.00 (Table 1).

Table 1
Sociodemographic characteristics of sex workers according to workplace. Brazil, 2009. (N = 2,523)

As for the characteristics of the study, those women who worked in indoor venues had spent a comparatively shorter time in prostitution and performed a higher number of sexual activities per day, as well as charging more (Table 2). As to the frequency of alcohol consumption, the differences between workplaces were statistically significant, at the 5% level of significance, with higher consumption among those women who worked in indoor venues (Table 2). Use of crack or merla was more frequently observed in women working on the streets. The declared percentage of cocaine used was high in both groups (Table 2). Whether cocaine was snorted or injected did not differ significantly according to workplace.

Table 2
Characteristics of work, alcohol and drug consumption in sex workers according to workplace. Brazil, 2009. (N = 2,523)

The results shown in Table 3 show the differences in accessing the health care system. In general, FSW working in indoor locations showed higher percentages of gynecological screening examinations and having been tested for syphilis at least once. However, there were no differences in receiving condoms or frequency of HIV testing.

Table 3
Access to health care and results of HIV and syphilis tests in sex workers according to workplace. Brazil, 2009. (N = 2,523)

There were some significant differences in the presence of sexually transmitted diseases (Table 3). The percentage of FSW on the streets with a syphilis serologic scar was 24.2%, almost 10 percentage points above those who worked in indoor locations (15.5%). The prevalence of HIV was also significantly higher among sex workers on the street (7.2%); twice as high as in the other group (3.6%).

Homophily was observed in the recruitment pattern according to workplace. The probability of a woman working in an indoor venue being recruited by another from an indoor venue was 65.4%, but the probability of being recruited by a woman working on the streets was only 34.6%, indicating homophily (Table 4). On balance, the estimated proportion of FSW from indoor venues is 59.0% and street workers 41.0%. Considering stratification by workplace, the weighted estimate of the prevalence of HIV was of 5.0%.

Table 4
Recruitment patterns of sex workers according to workplace. Brazil, 2009.

The tendency to recruit peers from the same stratum by workplace is illustrated in the Rio de Janeiro network (Figure).

Figure
Network of female sex workers who participated in the study according to workplace. Rio de Janeiro, RJ, 2009. (N = 601)

DISCUSSION

The results show differences in the FSW profiles according to workplace. Women who work on the streets had a higher probability of becoming infected with HIV. Older women with lower levels of schooling and income who work on the streets and who have spent longer in prostitution were associated with higher risk of becoming HIV infected, as has been discussed by other authors.2020  Li J, Chen XS, Merli MG, Weir SS, Henderson GR. Systematic differences in risk behaviors and syphilis prevalence across types of female sex workers: a preliminary study in Liuzhou, China. Sex Transm Dis. 2012;39(3):195-200. DOI:10.1097/OLQ.0b013e31823d2e2a A recent study1313  Hao C, Liu H, Sherman SG, Jiang B, Li X, Xu Y, et al. Typology of older female sex workers and sexual risk for HIV infection in China: a qualitative study. Cult Health Sex. 2014;16(1):47-60. showed that FSW aged 50 and over, as well as having been exposed for a longer time, having spent more years in the profession, are also more likely to have experienced unsafe sexual practices. The findings of this study show that FSW working on the streets had less access to the health care system. The coverage of cervical cancer screening among FSW in indoor venues in the three years preceding the research was 61.8%, lower than that of the 18 to 69-year old Brazilian female population (77.3%), (estimated using data from the 2008 PNAD – National Household Survey Health Care Supplementbb Instituto Brasileiro de Geografia e Estatística. Pesquisa Nacional por Amostra de Domicílios: um panorama da saúde no Brasil. Acesso e utilização dos serviços, condições de saúde e fatores de risco e proteção à saúde 2008. Rio de Janeiro; 2010 [cited 2012 Dec 5]. Available from: http://www.ibge.gov.br/home/estatistica/populacao/panorama_saude_brasil_2003_2008/PNAD_2008_saude.pdf). In FSW who worked on the streets, coverage was lower still; only 53.0%.

The amount the women charged was shown to be a relevant factor, being significantly lower among those who worked on the street. According to the amount charged, the clients differed regarding level of schooling and knowledge of HIV transmission,1010  Damacena GN, Szwarcwald CL, Barbosa Jr A. Implementation of respondent-driven sampling among female sex workers in Brazil, 2009. Cad Saude Publica. 2011;27(Suppl 1):S45-55. DOI:10.1590/S0102-311X2011001300006,2929  Zhang C, Li X, Hong Y, Zhou Y, Liu W, Stanton B. Unprotected sex with their clients among low-paying female sex workers in southwest China. AIDS Care. 2013;25(4):503-6. DOI:10.1080/09540121.2012.726345 frequently demanding unprotected sex, offering more money for this.1616  Kathleen EW, Eric JTT, Jay GS, Megan BM. How does sex trafficking increase the risk of HIV infection? An observational study from Southern India. Am J Epidemiol. 2013;177(3):232-41. DOI:10.1093/aje/kws338 The FSW, in turn, are not able to negotiate safe sex as they need the money.1919  Lau JT, Tsui HY, Siah PC, Zhang KL. A study on female sex workers in southem China (Shenzhen): HIV-related knowledge, condom use and STD history. AIDS Care. 2002;149(2):219-33. DOI:10.1080/09540120220104721

Charging low prices and the possibility of unprotected sex due to clients’ demands are among the main variables associated with HIV prevalence.1111  Damacena GN, Szwarcwald CL, Souza-Jr PRB, Dourado I. Risk factors associated with HIV prevalence among female sex workers in 10 Brazilian cities. J Acquir Immune Defic Syndr. 2011;57(Suppl 3):144-52. DOI:10.1097/QAI.0b013e31821e9bf6 Empowering women to negotiate safe sex with partners is considered to be one of the most relevant interventions in reducing HIV transmission in FSW.9 Chersich MF, Luchters S, Ntaganira I, Gerbase A, Lo YR, Scorgie F, et al. Priority interventions to reduce HIV transmission in sex work settings in sub-Saharan Africa and delivery of these services. J Int AIDS Soc. 2013;16(1):17980. DOI:10.7448/IAS.16.1.17980

Using crack was another factor which proved to be more relevant in street FSW. Studies have shown that drug abuse is associated with a significantly higher risk of becoming infected with HIV, as it can influence unsafe sexual practices.2323  Medhi GK, Mahanta J, Kermode M, Paranjape RS, Adhikary R, Phukan SK, et al. Factors associated with history of drug use among female sex workers (FSW) in a high HIV prevalence state of India. BMC Public Health. 2012;12:273. DOI:10.1186/1471-2458-12-273 The need for money to buy drugs is another factor which affects negotiations for safe sex.8 Campbell AN, Tross S, Dworkin SL, Hu MC, Manuel J, Pavlicova M, et al. Relationship power and sexual risk among women in community-based substance abuse treatment. J Urban Health. 2009;86(6):951-64. DOI:10.1007/s11524-009-9405-0,2424  O’Reilly JM, Hubbard ML, Lessler JT, Biemer PP, Turner CF. Audio and video computer assisted self-interviewing: preliminary tests of new technologies for data collection. J Off Stat. 1994;1092:197-214. A study reviewing articles on FSW in Central Asia concluded that the HIV transmission risk factor was the use of illicit drugs, both injectable and non-injectable.2 Baral S, Todd CS, Aumakhan B, Lloyd J, Delegchoimbol A, Sabin K. Literature review of HIV among female sex workers in the Central Asian Republics, Afghanistan, and Mongolia: contexts and convergence with drug use. Drug Alcohol Depend. 2013:132(Suppl 1):13-6

The results of this study also show that women who meet their clients on the street are more subject to sexually transmitted infections and have a higher prevalence of syphilis and HIV. The difference in syphilis serologic scars was almost 10 percentage points higher among those who worked on the streets, corroborating the findings of other studies.2020  Li J, Chen XS, Merli MG, Weir SS, Henderson GR. Systematic differences in risk behaviors and syphilis prevalence across types of female sex workers: a preliminary study in Liuzhou, China. Sex Transm Dis. 2012;39(3):195-200. DOI:10.1097/OLQ.0b013e31823d2e2a,3030  Zhou Y, Li X, Zhang C, Tan G, Stanton B, Zhang X, Cui Y. Rates of HIV, syphilis, and HCV infections among different demographic groups of female sex workers in Guangxi China: Evidence from 2010 national sentinel surveillance data. AIDS Care. 2013;25(11):1433-41.DOI:10.1080/09540121.2013.772282

Findings in the international literature corroborate the results depicted here, indicating that FSW on the streets are those most at risk of becoming infected with HIV.2121  Li Y, Detels R, Lin P, Fu X, Deng Z, Liu Y, et al. Difference in risk behaviors and STD prevalence between street-based and establishment-based FSWs in Guangdong Province, China. AIDS Behav. 2012;16(4):943-51. DOI:10.1007/s10461-011-0102-0 Moreover, differing attitudes and practices emphasize the need for studies which take into account separation according to workplace, to properly guide prevention and care actions for FSW.4 Blankenship KM, Burroway R, Reed E. Factors associated with awareness and utilisation of a community mobilisation intervention for female sex workers in Andhra Pradesh, India. Sex Transm Infect. 2010;86(Suppl 1):69-75.,7 Buzdugan R, Copas A, Moses S, Blanchard J, Isac S, Ramesh BM, et al. Devising a female sex work typology using data from Karnataka, India. Int J Epidemiol. 2010;39(2):439-48. DOI:10.1093/ije/dyp351,2020  Li J, Chen XS, Merli MG, Weir SS, Henderson GR. Systematic differences in risk behaviors and syphilis prevalence across types of female sex workers: a preliminary study in Liuzhou, China. Sex Transm Dis. 2012;39(3):195-200. DOI:10.1097/OLQ.0b013e31823d2e2a,2121  Li Y, Detels R, Lin P, Fu X, Deng Z, Liu Y, et al. Difference in risk behaviors and STD prevalence between street-based and establishment-based FSWs in Guangdong Province, China. AIDS Behav. 2012;16(4):943-51. DOI:10.1007/s10461-011-0102-0

As it uses peer recruitment techniques, in which the participant invites others with similar characteristics, the RDS method is recognized as probabilistic sampling which enables recruitment of individuals in populations to which it is difficult to gain access.2222  Malekinejad M, Johnston LG, Kendall C, Kerr LR, Rifkin MR, Rutherford GW. Using respondentdriven sampling methodology for HIV biological and behavioral surveillance in international settings: a systematic review. AIDS Behav. 2008;12(4Suppl):105-30. DOI:10.1007/s10461-008-9421-1 In Brazil, as well as enabling gaps in information concerning the FSW population to be filled, using RDS enables estimates of parameters to be calculated in order to monitor the HIV epidemic in this population subgroup.1010  Damacena GN, Szwarcwald CL, Barbosa Jr A. Implementation of respondent-driven sampling among female sex workers in Brazil, 2009. Cad Saude Publica. 2011;27(Suppl 1):S45-55. DOI:10.1590/S0102-311X2011001300006,1111  Damacena GN, Szwarcwald CL, Souza-Jr PRB, Dourado I. Risk factors associated with HIV prevalence among female sex workers in 10 Brazilian cities. J Acquir Immune Defic Syndr. 2011;57(Suppl 3):144-52. DOI:10.1097/QAI.0b013e31821e9bf6,2828  Szwarcwald CL, Souza-Jr PRB, Damacena GN, Barbosa-Jr A, Kendall C. Analysis of data collected by RDS among sex workers in 10 Brazilian cities, 2009: estimation of the prevalence of HIV, variance, and design effect. J Acquir Immune Defic Syndr. 2011;57(Suppl 3):129-35 DOI:10.1097/QAI.0b013e31821e9a36

As to the use of the RDS methodology, the findings indicate that FSW on the street recruit FSW who work in indoor venues, and vice-versa, with the networks not being independent. However, attention should be paid to the existence of homophily, especially concerning the tendency of participants from indoor venues to recruit peers from the same group. Firstly, it indicates the need to choose seeds diversified by type of workplace. Secondly, it emphasizes the need to incorporate the dependency of observations produced by the recruiting pattern in the statistical analysis. Lastly, and perhaps most importantly, the sample size should be sufficiently large to estimate the probabilities of transition from one state to another. As the homophily effect did not occur in FSW working on the street, but only in those working in indoor venues, the network developed more quickly among FSW in indoor venues.

Considering the transference process of sampling methods in populations to which it is difficult to gain access, conducted by the Global AIDS Program, Centers of Disease Control, a pilot study in Brazil, conducted in the city of Santos, SP, Southeastern Brazil, used the RDS method to select 173 FSW. Of these, 121 (70.0%) worked in nightclubs, of which 116 (96.0%) were concentrated in just two clubs.3 Barbosa-Jr A, Pascom ARP, Szwarcwald CL, Kendall C, McFarland W. Transfer of sampling methods for studies on most-at-risk populations (MARPs) in Brazil. Cad Saude Publica. 2011;27(Suppl 1):36-44. DOI:10.1590/S0102-311X2011001300005  As the network developed more quickly among FSW in indoor venues, the sample size needed to estimate the probability of transition and the proportions of FSW according to workplace was not reached, probably resulting in underestimation of HIV prevalence.

This limitation does not apply to this study, as the sample was sufficient to achieve Markov equilibrium and the homophily effect did not affect the estimated HIV prevalence. The estimate was very close to what had been found previously,2828  Szwarcwald CL, Souza-Jr PRB, Damacena GN, Barbosa-Jr A, Kendall C. Analysis of data collected by RDS among sex workers in 10 Brazilian cities, 2009: estimation of the prevalence of HIV, variance, and design effect. J Acquir Immune Defic Syndr. 2011;57(Suppl 3):129-35 DOI:10.1097/QAI.0b013e31821e9a36 even using the procedure of post-stratification according to workplace.

To conclude, the results suggest that strategies in the health care sector should increase access to and use of health care services, reducing inequality in coverage of gynecological examinations and regular syphilis testing; increase distribution of condoms, especially among the poorest FSW, so that they do not need to buy condoms; focus interventions on areas where FSW and clients with lower socioeconomic status are concentrated, where the FSW charge low prices; and empower the women to negotiate safe sexual practices.

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  • This study was supported by the Ministry of Health/Secretariat of Health Surveillance/Department of STD, AIDS and Viral hepatitis, through the International Technical Cooperation Project AD/BRA/03/H34 between the Brazilian Government and the United Nations Office on Drugs and Crime – UNODC (TC/CFA/CSV - 239/2007).
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    Instituto Brasileiro de Geografia e Estatística. Pesquisa Nacional por Amostra de Domicílios: um panorama da saúde no Brasil. Acesso e utilização dos serviços, condições de saúde e fatores de risco e proteção à saúde 2008. Rio de Janeiro; 2010 [cited 2012 Dec 5]. Available from: http://www.ibge.gov.br/home/estatistica/populacao/panorama_saude_brasil_2003_2008/PNAD_2008_saude.pdf
  • Article based on the doctoral thesis of Damacena GN, entitled: “Análise de dados coletados por respondent-driven sampling (RDS): um estudo da prevalência de HIV e fatores associados entre mulheres trabalhadoras do sexo em 10 cidades brasileiras.” presented to the Escola Nacional de Saúde Pública Sérgio Arouca of the Fundação Oswaldo Cruz, in 2012.

Publication Dates

  • Publication in this collection
    June 2014

History

  • Received
    13 June 2013
  • Accepted
    21 Oct 2013
Faculdade de Saúde Pública da Universidade de São Paulo São Paulo - SP - Brazil
E-mail: revsp@org.usp.br