Introduction
Sex work has long been recognized as a driver of epidemics of sexually transmitted infections (STIs), including HIV, in several Asian settings [1,2]. These epidemics are initially concentrated among sex workers and generalized among clients and their partners; these groups, predominantly sex workers, have been the target of prevention activities in settings in which sex work is openly conducted [3–5]. In more conservative settings such as Pakistan and Iran, sex workers remain a largely hidden population [6,7]. HIV has been documented among sex workers in these settings and concern is growing that this population will be difficult to reach with prevention activities [7,8].
In Afghanistan, sex work is illegal and, in prior governments, was a capital offense [9,10]. However, sizable sex worker populations have been enumerated in several urban centers [11,12]. This risk group is predicted to increase in size due to rising living costs and limited job prospects, particularly for women [10]. Men, particularly adolescent boys, also engage in sex work and transactional sex [11]. As noted in other settings, there is some degree of overlap between drug user and sex worker populations, which increases direct risk of HIV infection for sex workers and establishes sex workers as a bridging group between injection drug users (IDUs) and other populations [13–15]. Among IDUs surveyed in Kabul in 2006, the majority reported ever having patronized a female sex worker (FSW) and condom use was rare [16].
Afghanistan is considered to be a low HIV prevalence country; however, there are few data regarding prevalence of STIs, such as Neisseria gonorrhea and Chlamydia trachomatis, among general population or vulnerable groups in Afghanistan. [1]. Among a national sample of 16 870 blood donors in 2005, positive screening tests were reported for hepatitis C virus (HCV) among 2.6%, for syphilis suggestive [venereal disease research laboratory (VDRL)] reaction among 0.35%, for hepatitis B surface antigen (HBsAg) among 1.23%, and for HIV among 0.12% [17]. Among a sample of obstetric patients in Kabul, there were no HIV or syphilis cases detected in 2006; the prevalence of HBsAg was 1.53% [18]. However, among IDUs in Kabul and Hirat, measurable prevalence of HIV (3.1% for both cities), HBsAg (6.5 and 3.5%), and syphilis (1.2 and 1.5%) was detected in 2005 and 2007, respectively [16,19,20]. Prior reports indicate that both HIV awareness and condom use are quite low among FSWs in Kabul, but there are no data on STI prevalence among this group [11,21]. The purpose of this study was to assess seroprevalence of HIV, syphilis, HCV, and hepatitis B virus (HBV) and associated risk behaviors among FSWs in three Afghan cities.
Methods
Setting
Participants were recruited in Jalalabad, Kabul, and Mazar-i-Sharif, the largest cities in their respective regions. Kabul, the capital of Afghanistan, has a population of 3.5 million, with Dari (Afghan dialect of Farsi) being the most common spoken language amidst an ethnically diverse population [22]. The population of Mazar-i-Sharif, approximately 300 600, is ethnically mixed with the predominant languages spoken being Dari and Uzbek [22]. Jalalabad is located in Nangahar province, with an estimated population of 60 000 and is predominantly Pashtun [22]. At the time of this study, there were two sex worker-focused programs operating in Kabul, with one program each in Jalalabad and Mazar-i-Sharif.
Study design and participants
This cross-sectional study was conducted between September 2006 and January 2008 through the designated programs or International Rescue Committee (IRC) study offices in each site. Eligible participants were those reporting sex work within the past 6 months, aged 18 years or greater, and able to provide informed consent. Prior to data collection, approval was obtained from the institutional review boards of the University of California, San Diego; the Walter Reed Army Institute of Research; the U.S. Naval Medical Research Unit 3 in Cairo, Egypt; and the Ministry of Public Health of the Islamic Republic of Afghanistan.
Measures
The study instrument assessed sociodemographics, travel, sex work histories, and other risky drug use and sexual behaviors. Duration of sex work, age of sex work initiation, travel outside Afghanistan, and monthly client volume were included to reflect potential exposure to infection. Condom use and consistent use with clients in the past 6 months were analyzed to assess for protective effect. We also assessed current STI symptoms and treatment for an STI in the past 3 months to provide additional insight into sexual risk and care-seeking behaviors. Illicit drugs and alcohol use were assessed, including whether drugs were used to facilitate sex work or used with clients.
Procedures
Only individuals previously identified as sex workers through outreach or other prior programs were considered for participation. Program outreach workers or employees of the aforementioned programs approached sex workers in their usual places of congregation (e.g. bazaars, tea houses) or the program office and briefly described the study. Those individuals interested in participation were invited to the program office or, where not possible, to the study office and met in a confidential room by a sex-matched study representative, where informed consent was obtained. The study questionnaire was then administered in either Dari or Pashto, according to the participant's preference, in a confidential setting by a sex-matched trained interviewer.
Rapid whole blood testing for HIV, syphilis, and HBsAg were performed with Determine HIV ½, Determine Syphilis, and Determine HBsAg (Abbott Diagnostics Japan, Tokyo, Japan), and hepatitis C virus antibody (HCV Ab) with Standard Diagnostics HCV Ab (Standard Diagnostics, Kyonggi-do, Korea). Positive HIV screens were assessed with a second rapid test, HIV (1+2) Antibody Colloidal Gold (KHB Kehua, Shanghai, China). Participants with positive rapid tests (and, in the case of HIV, any discordant results with the two rapid tests) underwent intravenous sampling for confirmatory serologic testing. Positive or discordant HIV rapid tests were confirmed with western blot assay (HIV Blot 2.2; GeneLabs Diagnostics, Singapore, Singapore). Syphilis was confirmed with Treponema pallidum particle agglutination (TPPA) assay (Fujirebio Diagnostics, Malvern, Pennsylvania, USA) and HCV Ab was confirmed with RIBA (RIBA 3.0 SIA; Chiron Corporation, Emeryville, California, USA), with testing performed at the Afghan Public Health Institute (APHI) Laboratory in Kabul. Participants were provided with follow-up appointments with the study team for confirmatory results. HBsAg was confirmed with PCR (Amplicor; Roche Diagnostics, Mannheim, Germany) at the NAMRU-3 laboratory in Cairo, Egypt.
All participants received pretest and posttest counseling and risk-reduction counseling, a small nonmonetary gift of hygiene items (e.g. toothpaste, shampoo) of US$8 value, and condoms. No data were recorded on those declining or ineligible for study entry. Participants with positive screening tests were provided with follow-up appointments to obtain confirmatory results. Syphilis treatment was available through the study program, whereas participants with hepatitis or HIV were provided with risk-reduction counseling and referred to the nearest voluntary counseling and testing (VCT) center for care.
Statistical analysis
Descriptive statistics for the study population were generated, stratified by study site. The outcomes of interest were infection prevalence and any detected associations with specific risk behaviors. Prevalence of HIV, syphilis, HCV, and HBV was calculated with 95% confidence intervals (CIs) based on Poisson and binomial distributions.
Continuous variables, such as duration of sex work, were transformed to dichotomous variables at the median. Risk behaviors, such as condom use with clients, were reported by frequency. These variables were dichotomized into ever/never (e.g. drug use) or always/not always (e.g. condom use with clients in the past 6 months). Correlates of HIV, HCV, and syphilis were not analyzed due to low prevalence. Site-controlled logistic regression was performed to identify potential associations between HBV and demographic and risk behavior variables. Variables were entered into a multivariable model if they were associated at the 10% level in univariable analysis. The final site-controlled multivariable model was inclusive of all variables either remaining significant or identified as confounders in the likelihood ratio test. The goodness-of-fit of the model was assessed with the Hosmer–Lemeshow test.
Results
Demographics
There were 543 sex workers enrolled in the study; due to the low number of male sex workers (n = 23), analysis was confined to FSWs (n = 520). The majority of FSWs had been married, had no formal education, and originated from Afghanistan (Table 1). Most had children, of whom 94.8% lived with their children. There were significant differences in sociodemographic characteristics by site, with FSWs from Jalalabad being younger, less likely to have been married, and more likely to have lived outside the country in the past 5 years (Table 1). Most (83.4%) participants were unemployed, with others reporting additional employment as cleaners, teachers, or other jobs.
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Table 1: Sociodemographic and behavioral characteristics of female sex workers in Afghanistan (n = 520).
Sex work-related characteristics
The mean ages of sexual debut and sex work initiation were 18.1 years (SD = 3.0) and 23.3 years (SD = 5.1), with 11.2% engaging in sex work prior to age 18. Overall, participants reported a mean of 16.9 [SD = 15.0, interquartile range (IQR) = 5–25] monthly clients, with an average service charge of 627 Afghanis (SD = 434; range: 100–3000; US$1 = 50 Afghanis). Of 710 responses (multiple answers allowed), the most common reasons for engaging in sex work were need to support herself (50.0%) or her family (32.4%); 8.9% reported being forced into sex work by their families. Few reported turning to sex work after being widowed (5.2%) or after being sexually assaulted and consequently unable to marry (1.5%). As FSWs could find clients through multiple sources, 960 responses were received for the question assessing where clients were met. The most common venues for meeting clients were at the bazaar (29.7%), by telephone (24.7%), or through a pimp or madam (24.2%); other venues reported were the tea house (chai khana; 12.6%) and private homes (7.9%).
Risky behaviors
Two-thirds of FSWs (63.3%) had heard of condoms, of whom only half (51.7%) had ever used a condom (Table 1). Nearly one-third (30.2%) of participants had ever used a condom with clients, with 60 (38.2%) reporting always using condoms with clients in the past 6 months. Of sexual services provided, most participants offered only vaginal intercourse (74.8%), with 18.7% providing both vaginal and anal sex, 2.7% anal sex only, and 2.5% oral and vaginal sex only. FSWs providing anal sex were more likely to have ever used condoms with a client (P = 0.005). Half (51.7%) of participants reported treatment for presumptive STI in the past 3 months; 29.8% (n = 155) reported genital sores, warts, or itching at the time of enrollment.
Regarding other risky behaviors, 6.9% reported ever having used nonmedicinal drugs, of whom 34.4% had used sedatives (e.g. diazepam), 28.1% had used pain medication (e.g. pentazocine hydrochloride), 9.4% had used opium, and 6.3% had used marijuana (64 total responses). Only two participants reported ever having injected drugs. Alcohol use (which is illegal in Afghanistan) was reported by 4.7% (n = 26 participants). Most participants who reported alcohol or drug use only used the substance sporadically, with 93.3% of alcohol users consuming three drinks or less each week and 76.2% using medications or other substances twice weekly or less. Of participants using drugs or alcohol (n = 51), most reported that alcohol (80.7%) and substance use (72.1%) made sex work easier and 53.9% reported using alcohol or drugs with clients.
Seroprevalence
Seroprevalence of the measured infections was relatively low, with only one case of HIV (0.19%, 95%CI 0.005–1.07) and no cases of syphilis detected. Ten participants had HCV (1.92%, 95%CI 0.92–3.54). HBV was the most common infection, with 34 cases (6.54%, 95%CI 4.41–8.67) diagnosed. There were significant differences by site for HBV prevalence, ranging from 3.0% in Mazar-i-Sharif to 17.5% in Jalalabad (P < 0.001).
Correlates of infection
The low prevalence of HIV, syphilis, and HCV precluded subsequent risk factor analysis. In univariable analysis, HBV was associated with ever using drugs, ever using alcohol, charging less than 450 Afghanis per service, at least 12 clients monthly, and having children (Table 2). In multivariable analysis, at least 12 clients monthly, ever using alcohol, provision of anal sex, and having children were independently associated with HBV infection (Table 3). No variable reflecting condom use was associated with HBV when considering the entire FSW population (data not shown).
Table 2: Factors associated with hepatitis B virus infection among 520 female sex workers in Afghanistan in site-controlled univariate logistic regression analysis.
Table 3: Factors independently associated with hepatitis B infection among female sex workers in three cities in Afghanistan (n = 520).
Discussion
Seroprevalence of HIV, syphilis, and HCV were low in these three FSW populations, as compared to IDUs, the only other vulnerable group for which data are available in this setting [16,19,20]. HBV prevalence was also relatively low and similar to that measured among Afghan refugees in Pakistan and among IDUs in Kabul [16,23]. The relatively higher prevalence of HBV in Jalalabad was also observed among IDUs recruited in that city; we attribute this to the proximity to Pakistan, where HBV is endemic and where border crossing was relatively easier than for other countries bordering Afghanistan at the time of this study [24]. In the case of FSWs, HBV exposure may be related to clients spending time in Pakistan. Jalalabad lies on key trucking routes for importation of goods from Pakistan, usually originating at the ports in Karachi [25]. Long-distance truckers have been identified as a bridging group for HIV in other Asian settings such as India, and Pakistan, and may be contributing to the higher prevalence of HBV among FSWs in Jalalabad [26,27]. However, as the prevalence of HBV in the general population in Jalalabad is unknown, it is possible that the disparity between sites represents chronic infection acquired either at birth, through household contacts, or iatrogenically remotely. HBV prevalence among general population groups in Jalalabad should be considered as results may influence childhood vaccination strategies.
HBV was independently associated with charging less for services and with providing anal sex. We believe these associations may result from practices driven by poverty or an increasing number of FSWs. Additionally, engaging in anal sex may be a means of preventing pregnancy in a situation in which there is no ability to negotiate condom use. Given the relatively large proportion of FSWs who were married at the time of the study, avoiding vaginal intercourse with clients might ensure there were no paternity disputes or other issues that might lead to an unsafe domestic situation. Anal sex as a means of avoiding unintended pregnancy has been described among adolescent populations, a vulnerable population often lacking condom negotiation skills [28,29]. Further study on the context of condom use with sex work in this setting is needed to better understand reasons for this observation.
The association between HBV and having children may reflect infection acquired at the time of delivery. Although assisted deliveries are slowly increasing in Afghanistan, most participants had lived or worked outside Afghanistan in the recent past and may have delivered while refugees [30]. Iatrogenic transmission through injections has been demonstrated to be a large contributor to prevalence of HBV and HCV in Pakistan [31,32]. This association might also reflect willingness of women with dependent children to engage in riskier behaviors or be less discriminating in their clientele and thus be at greater risk for infection.
Ever using alcohol was independently associated with HBV infection in multivariable analysis as was ever using drugs in univariable analysis; these associations may reflect a compromised ability to negotiate condom use when intoxicated. Although drug or alcohol use was uncommon among participants, those who had used either substance believed that sex work was easier while intoxicated, an opinion shared by FSWs in diverse settings such as Vietnam, the Philippines, and Mexico [33–35]. Use of alcohol or drugs to cope with sex work may increase the likelihood of engaging in risky sexual behaviors or having clients who are drug users, as substance use with clients was reported by half of FSWs who had used drugs or alcohol.
Although there is little information regarding the context of sex work in Afghanistan, the characteristics reported by our participants indicate several general differences from those reported among FSWs in Kabul in 2002 [11]. Generally speaking, the reported average number of clients and price/service has decreased, whereas the use of gatekeepers to find clients has increased. The latter finding is supported by our data that nearly one-fourth of women found clients through gatekeepers (i.e., pimps or madams). Our data also speak to how few alternative employment opportunities exist for women in Afghanistan: over four-fifths of women had no other employment, the majority engaged in sex work to support themselves or their families, of whom 5% were widows, and nearly one in 10 were forced to participate in sex work by their families.
There are a number of limitations to these data that must be considered. First, due to convenience sampling, the results may not represent the true prevalence of HIV, HCV, HBV, or syphilis among FSWs in the cities assessed. Our efforts to safely access this hidden population through outreach programs likely prevented complete representation of FSWs in those cities, but were necessary for participant and staff safety. Although methodologically suboptimal, input following ethical review for this first study among sex workers in Afghanistan determined that recruitment performed solely among previously identified sex workers through operating sex worker-oriented programming optimally minimized participant risk. We also attempted to recruit male sex workers, but could not accrue a sufficient number for characterization; only 23 were enrolled. Further, only adults (age of majority in Afghanistan is 18 years) were considered for participation, though at least 10% of the participants initiated sex work prior to that age. Male and child sex work has been reported in Afghanistan and may have very different associated risk behaviors and resulting prevalence of STIs [11]. Analysis of factors associated with HIV and HCV was underpowered due to the very low prevalence of these infections, potentially masking some associations. Face-to-face interviews may have resulted in socially desirable responding regarding various risky behaviors. We attempted to minimize this by having same-sex interviewers; self-administered questionnaires were not feasible due to low literacy and the costs of interactive audio programs were prohibitive. Last, participants were enrolled based on self-report of engaging in sex work. As there were no objective means of determining FSW status, we note that some individuals may have been enrolled who had not actually engaged in sex work. However, monitoring of staff performance, intensive training/re-training, and use of nonmonetary incentives were employed to minimize this occurrence.
In conclusion, although prevalence of HIV, HCV, and syphilis are low among FSWs in Jalalabad, Kabul, and Mazar-i-Sharif, Afghanistan, risky sexual behaviors were common and condom use rare. A number of factors, both social and economic, favor an increasing number of women turning to sex work for survival and create an environment favorable to infection transmission. In addition to vocational training and educational opportunities for women and political advocacy for women's rights, outreach programming for FSWs should emphasize health sexual education and techniques for culturally informed condom negotiation. Further, healthcare, including counseling and HIV/STI testing, reproductive healthcare, and hepatitis B vaccination, should be incorporated with FSW-oriented outreach programming.
Acknowledgements
We thank the Ministry of Public Health, the Action Aid/University of Manitoba study team, and ORA/KOR program for their assistance. We thank our participants for their time and trust. We thank Ms. Kathy Fiekert for her assistance with data entry management. This study is dedicated to the memory of Boulos Botros, DVM, PhD.
The present study was funded by the Walter Reed Army Institute of Research. The opinions and assertions made by the authors do not reflect the official position or opinion of the U.S. Department of the Navy or Army, or of the respective in-country National HIV/AIDS Control Programs and other Non-Governmental Organizations (NGOs). C.S.T. appreciates support from the Fogarty International Center of the National Institutes of Health (K01TW007408).
The research study experienced a 6-month lapse of NAMRU-3 IRB approval; this lapse occurred following completion of participant enrollment.
Partial results have been presented at the International AIDS Conference in Mexico City, Mexico, in August 2008 and in the publication, SAR AIDS Human Development Sector, South Asia Region, The World Bank. Mapping and Situation Assessment of Key Populations at High Risk of HIV in Three Cities of Afghanistan. Available at:siteresources.worldbank.org/INTHIVAIDS/Resources/-2008-05-16.For the latter publication, the data provided were at the mid-point in the collection process.
Conflicts of Interest: None.
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