Sex work is a universal phenomenon, existing in all cultures and throughout history [1,2]. Yet, sex work is illegal in most nations and severely punished in many . The varied context of sex work, including its relative visibility and societal tolerance, results in wide variation in the prevalence of HIV and STI, and in the dissemination and practice of preventive measures from country to country and region to region [3–5]. According to WHO and UNAIDS statistics, HIV prevalence among sex workers ranges from 0.2% to 60.5% in sub-Saharan Africa, 0% to 26.0% in South and South East Asia, and 0% to 14.0% in Latin and Central America and the Caribbean [1–9]. Worldwide, female sex workers (FSW) are regarded as one of the populations affected early and disproportionately in low-level and concentrated HIV epidemics (prevailing in many countries of the Middle East and North Africa) and remain with elevated HIV prevalence in generalized epidemics (as is the situation in sub-Saharan Africa) . However, few specific data are available for FSW in Sudan, a large country that spans these sweeping macroregions.
In recent years, the Sudan National AIDS Program has raised the priority of interventions among the often-called most-at-risk populations (MARPs) with particular emphasis on FSW. The lack of data on MARPs in general and FSW in particular, in north Sudan hinders their development. To date, only one survey conducted in 2002 included HIV prevalence among FSW, producing a national estimate of 4.4%  – a figure that nearly breaches the 5% threshold defining a concentrated epidemic. The same survey ominously documented very low ever use of condoms, under 4%, among FSW. More up to date data and a more systematic approach to including FSW and other MARPs into routine HIV surveillance efforts are needed in Sudan if prevention efforts are to succeed in stemming the wider spread of infection.
As a first step in establishing an integrated biological and behavioral surveillance (IBBS) system for MARPs in Sudan, we conducted a respondent-driven sampling (RDS) survey among FSW in Khartoum. The primary aims of the study were to measure the prevalence of HIV infection and other standardized indicators of HIV-related risk behaviors, HIV/AIDS knowledge, and use of preventive services. The broader goal was to assess and provide sound information and recommendations that will guide the interventions among FSW in the country.
This study was conducted in Khartoum State, which includes the capital and largest metropolitan area of Sudan, located in the north of the country. According to the Fifth Sudan Population and Housing Census of 2008, the total population of Khartoum was 5 274 321 . The city is subdivided into three major towns and seven administrative localities.
Study design, study individuals, and sampling methods
We conducted a cross-sectional survey using respondent-driven sampling (RDS) to reach and recruit the target population of FSW in Khartoum from April to May of 2008 [13,14]. Inclusion criteria were being paid for sex during the last 3 months, age 18–49 years, living in Khartoum State at least for 1 year, and, in accordance with the RDS methodology, having been recruited by an FSW peer from their social network. Seven seeds were identified by outreach worker/interviewers during a formative phase to initiate recruitment chains. After completing all study steps, each respondent was given three coupons used to recruit her peers. The chains of recruitment continued until the sample size was met and equilibrium was achieved on basic demographic characteristics. FSW referred their peers to the study site, which was a conveniently located private apartment. At the site, women presenting with recruitment coupons were assessed for eligibility and informed consent was conducted. FSW were reimbursed $10 for their transportation costs and time in completing the survey and $10 for each eligible FSW they referred. Recognizing the vulnerability of the target population, participation was anonymous, voluntary, and precautions were taken to protect the study respondents. Internal review board (IRB) approval was obtained from the federal research ethical committee at the Ministry of Health.
A standardized questionnaire for use in high-risk populations by the Sudan National AIDS Program was adapted from the female sex worker module of the Family Health International Behavioral Surveillance Surveys . The structured questionnaire included sociodemographic characteristics, knowledge about HIV/AIDS, condom use and accessibility of condoms, sexual behavior, drug use, and access and utilization of HIV-related services. Interviewers administered the surveys face-to-face.
After completion of the survey, venous blood samples were collected from respondents consenting to HIV testing. From the samples, dry blood spots (DBS) were prepared and stored in required conditions. All specimens were tested at the National Health Laboratory using the approved algorithm of two ELISA tests run sequentially. In the first screening test, we used Vironostika HIV Ag/Ab (BioMerieux, Boxtel, The Netherlands). All reactive specimens were retested by Enzygnost Anti-HIV ½ plus (Siemens Healthcare Diagnostics Products GMBH, Marburg, Germany). Specimens were considered positive upon confirmation by the second test.
Data were entered into SPSS V 11.5 for Windows, cleaned and checked for completeness, correct range responses, internal consistency, and reliability against the original data forms. The data file was exported to RDSAT 5.6.0 where univariate analyses were performed to generate population prevalence estimates and 95% confidence intervals (CI) for each variable.
The initial seven seeds ultimately reached 537 individuals through their social networks. Of these, a reported 118 declined to accept the recruitment coupons and 88 presenting to the study site were ineligible. Only three eligible respondents refused to participate in the study. The final sample included 321 FSW who completed both behavioral and serological steps of the study.
The population estimates (i.e., adjusted for the RDS design) for demographic characteristics are presented in Table 1. The majority (67.9%) was younger than 28 years and nearly one in four (23.5%) had no education at all. Most of the respondents (73.4%) had been married or cohabited with a man. Of these, 71.3% were currently married or cohabiting. About half (51.0%) of those ever married were married before reaching 18 years of age. Almost all respondents were Sudanese nationals and Muslim, 99.7% and 90.2%, respectively. Most (73.3%) were supporting dependent family members and only 28.5% had jobs other than sex work. The majority (86.2%) reported financial need as the reason for entering sex work.
Table 2 presents HIV prevalence and risk-behavior indicators. Overall, three women tested positive for HIV giving a population prevalence of 0.9% (95% CI 0.1–2.2). More than one-fifth (21.6%) had their first sexual intercourse before the age of 15 years. Nearly one-third (31.0%) began selling sex as a child (under 18 years old). The majority (60.6%) spent less than 5 years selling sex. About one-fifth (18.8%) reported eight or more nonregular or paying partners in the last 7 days. Only 30.9% had one client in their last working day, whereas the rest had multiple clients. In addition, 27.6% had five or more sexual act with the same most recent client over the last 30 days. Less than half (45%) used condom at their last sexual act with a client and only 35.9% reported consistent condom use with all clients in the last 30 days. The three most common reasons cited for not using a condom at last commercial sex were did not think of it (34.3%), partner refused (21.8%), and using of other contraceptive methods (18.8%).
Table 3 presents HIV prevention knowledge. Although 98.4% of the respondents heard of AIDS, 68.8% of them managed to identify that AIDS can be transmitted through anal sex and only 25.4% showed comprehensive knowledge. On the contrary, 73.7% knew where they could obtain a condom. In response to self-assessment of the risk of contracting the AIDS virus, 42.9% considered themselves at low or no risk. Finally, only 7.0% of respondents had previously tested for HIV and got the result during the last 12 months.
HIV prevalence among FSW in this first RDS survey conducted in Sudan was just under 1%. Fortunately for the present, the estimate (0.9%) and the associated upper bound confidence limit (2.2%) are below the 5% level that is held as a threshold for a most-at-risk population (MARP) in defining a concentrated epidemic. This estimate for Khartoum in the north of Sudan is below the previously estimated 4.4% HIV prevalence for FSW in the national situation analysis of 2002  and well below the 16.0% HIV prevalence measured in Juba in the south of Sudan in the 1990s . Our estimate falls near the lower range of HIV prevalence among FSW in the region of sub-Saharan Africa (0.2–60.5%) , but typical for the region of the Middle East and North Africa exclusive of Djibouti, Somalia, and south Sudan .
Many features of sex work appear universal, and our survey shows that Sudan is no exception. For example, that two-thirds of FSW in our study were younger than 28 years is consistent with data from Eastern Europe and Latin America [17,18], although higher than the approximately half of women suggested by a recent qualitative investigation in Khartoum . Of great seriousness is the young age of first selling sex found in our study; nearly one-third entered the sex trade in Khartoum as a child, a finding similar to a high intensity brothel setting in India . Our survey documented lower condom use at last sex with clients and consistently in the last month (45.0 and 35.9%, respectively) compared with recent reports from neighboring Ethiopia and Kenya [21,22], but suggests some improvement over the less than 4% estimate in the national assessment survey of 2002 . Client refusal to use condoms ranked low among the reasons for not using condom, lower than Argentina, for example, where 87% responded that clients preferred not to use condom . Surprisingly, more than one-third of our respondents claimed they did not think of condoms at the time of intercourse with their clients and about one-fifth used another contraceptive method. On the contrary, about one-tenth reported not using condom because of unavailability. These findings might reflect perception rather than accessibility issues around condoms and condom use. Our findings suggest that the levels of basic HIV prevention knowledge, perception of risk, and uptake of preventive services are relatively low among FSW in Khartoum. Although only one in four FSW in our study could show comprehensive knowledge of HIV prevention, this figure is twice as high as in Ethiopia . On the contrary, the low uptake of voluntary HIV testing could be explained in part by the low perception of risk, as only one in five considered herself at high risk. Again, as the HIV testing figure is disappointingly low, there appears to be some improvement since 2002 when only 0.4% of FSW had tested and obtained results . FSW-friendly facility-based and mobile voluntary testing services are needed to more rapidly fill this gap.
As typical around the world, we also found few women had another source of income whereas most were supporting family members. Models for HIV prevention among sex workers therefore need to foster economic independence with alternative income generation skills. Lessening the exclusive dependency on sex work for survival should strengthen the position to negotiate condom use. Encouragingly, the majority of our respondents had spent less than 5 years as sex workers, an opportunity for intensifying behavioral change interventions and income generation activities to minimize exposure and shorten the duration in the field of sex work.
Our survey also found substantial evidence for transmission to and from other populations. First, the turnover of risky partners (nonregular partners and clients) was moderately high, with nearly 40% having more than three in the last week, and most women (69.1%) having multiple clients on their last working day with 10% having more than five clients. Second, a considerable proportion of our respondents had regular partners, with nearly three-quarters ever married or cohabiting and two-thirds currently married or cohabiting. Such findings are particularly disturbing, as they show dual bridging to the regular partners of both FSW and clients of FSW. As the current interventions are focusing mainly on FSW, the challenge facing prevention interventions will be on how to reach clients of FSW and their regular partners as well as the regular partners of FSW themselves.
We are aware that each study has its limitations. In our case, we anticipated that a few noneligible participants would be included because recruitment depended on recruiters’ and recruits’ self-identification and due to the moderate incentive for participation. To minimize such bias, we used a well trained research assistant with extensive experience in working among FSW for an initial screening based on a brief interview. A second screening took place during the questionnaire where trained interviewers detected inconsistencies in responses and unfamiliarity with terms. Through this process, we manage to exclude 88 ineligible respondents. Another limitation is that our sample may not have reached all social networks of FSW in Khartoum. Although a purported strength of RDS is its ability to penetrate deep into diverse social networks [13,14], this is hard to verify. For example, the proportion of non-Sudanese participating appears low, perhaps as a result the severe legal consequences of selling sex and its implication on the residence status of non-Sudanese FSW.
Our finding of relatively low HIV prevalence for sex worker populations in the developing world should not be cause for complacency in HIV prevention. Although lower than the conventional 5% cut-off for concentrated epidemics, our HIV prevalence figure is five times higher than observed among pregnant women attending antenatal clinics in 2007 . Moreover, structural factors present in Sudan (e.g., the economic status of women, severe stigma and legal consequences of sex work) may engender further spread of HIV. The numbers of client and regular partners, the levels of unprotected sex with each, the poor prevention knowledge, and low uptake of preventive services all point to a fragile situation that may change rapidly for the worse. A high level of vigilance in HIV surveillance among FSW is therefore required. We found that, despite limitations, the RDS approach was logistically feasible and an appropriate match to the setting of FSW in Sudan where data are urgently needed to advocate for very basic prevention programs if prevalence in the north of the country is to remain low.
The support of TDR/WHO-EMRO for partially funding this study and the WHO Sudan Office for bridging the funding gap are gratefully acknowledged. The Sudan National AIDS Programme and the National Health Laboratory at the Federal Ministry of Health for conducting biological testing to our study specimens are recognized as vital to this project's success. Support for analysis and manuscript preparation was provided in part by the American University of Beirut and the WHO-EMRO office. We are indebted to Willi McFarland for his valuable editorial assistance and guidance. This study would also not have been possible without the sincere dedication, patience, and enthusiasm of the field research team, Ms. Sara, Ms. Shama, Ms. Amal, Ms. Bakhita, Ms. Arafa, and Mr. Mohammed, and the courage of Mr. Anas. Above all, thanks is due to the study respondents for their willing participation, trust in our team, and for giving us access to their personal information.
This study is funded by the TDR-WHO-EMRO and WHO-Sudan Office
Conflicts of Interest: None.
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