BOTH INTRAVENOUS DRUG USERS and commercial sex workers are potentially at great risk of contracting and transmitting HIV and other serious infections. Female sex workers (FSWs) who also inject drugs could therefore be at especially high risk. The close links between drugs and prostitution have been known for many years. Many FSWs in developed countries inject drugs and are HIV-infected. 1,2 In the United States and Europe, parenteral drug abuse has been a major route of HIV transmission among FSWs. 3 Within European and North American countries, HIV prevalence among FSWs has been closely associated with intravenous drug use and sharing of injecting equipment. 4–6 HIV prevalence is high in drug users in Thailand, Malaysia, southern China, Myanmar, Vietnam, and northeast India, few of whom are sex workers. Infection in FSWs in these countries was therefore initially the result of sexual relations with drug users, not of injecting among FSWs, which was rare until 1997. 7–13
Until 1998, HIV infections in Vietnam occurred primarily among male intravenous drug users, 14 although sentinel surveillance data showed that the prevalence of HIV infection among FSWs increased slowly from 1994 to 1998, primarily in the southwest. The prevalence increased rapidly from 4% and 3% in 1998% to 16% and 7% in 1999 in Ho Chi Minh City and Hanoi, respectively. The prevalence continued to increase to 18% and 10% in the year 2000 for Ho Chi Minh City and Hanoi, respectively. No data regarding drug injecting among FSWs had been collected in Vietnam, but informal observations suggested that some FSWs are injecting drugs. Therefore, we initiated a study of intravenous drug use and HIV infection among streetwalking sex workers (SSWs), the lowest paid and presumably highest-risk sex workers in Ho Chi Minh City.
Methods
A cross-sectional study was conducted in Ho Chi Minh City during December 2000. Sites frequented by SSWs were mapped by trained peer educators. SSWs identified in these sites in the mapping phase were invited to visit 1 of 3 sexually transmitted disease (STD) clinics for commercial sex workers in Ho Chi Minh City. Among 425 SSWs who were invited from all sites, 398 (94%) participated in the study. Participants were given 40,000 VND ($2.50 US) compensation. After verbal informed consent was obtained, an anonymous questionnaire about sociodemographic characteristics, sex partners, condom use, STD symptoms, and history and knowledge about and attitudes toward HIV/AIDS was administered face-to-face. Questions about previously being tested for HIV and exposure to HIV/AIDS prevention intervention were also asked. The questionnaire was pilot-tested for accuracy and cultural sensitivity. The interviewers were health workers who had been trained during a 2-day session. No identifying information was collected. At the end of the interview, the participants were asked to provide 4 mL of blood. All blood samples were processed at the Center for Preventive Medicine in Ho Chi Minh City. Sera were sent to the reference HIV laboratory of the National Institute of Hygiene and Epidemiology for HIV testing. HIV antibodies were assessed by the enzyme linked immunosorbent assay test according to the HIV testing strategy III recommended by the World Health Organization (WHO, 1992).
Data were entered using the EPI-INFO 6.12 program (http://www.cdc.gov/epo/epi/epiinfo.htm ). Univariate associations were evaluated using chi-squared tests and the Student t -test for continuous variables using the 2-sided test for level of significance. To determine which variables were independently associated with outcomes, logistic regression was performed. Selection of variables into the logistic model was based on prior knowledge and the magnitude of the risk ratios in univariate analysis. For highly correlated variables, only one representative variable was selected. The selected variables were entered in the regression model using the logistic model of PC-SAS to determine level of significance.
This study was reviewed and approved by the Institutional Review Board of the National Institute of Hygiene and Epidemiology, Hanoi.
Results
Sociodemographic Characteristics
The mean age of the participants was 31 years (range, 15–56 years). Over half had less than 6 years of education or were illiterate. Most of the SSWs were born in Ho Chi Minh City (86.3%). The prevalence of HIV was 16.3%. Approximately 28% currently lived with a husband/lover. The mean age of first selling sex was 25.2 years (range, 13–30 years). Almost 13% (12.8%) of the SSWs injected drugs. A higher proportion of injecting SSWs were illiterate (P = 0.001) (Table 1 ). A lower proportion of injecting-drug SSWs were married (P = 0.001). A higher proportion of injecting-drug SSWs had been in the rehabilitation center for commercial sex workers (P = 0.02) and had entered the rehabilitation center for drug users (P = 0.001). Drug-injecting SSWs had fewer years in prostitution than the non-injecting drug SSWs (P = 0.0004).
TABLE 1: Sociodemographic Characteristics of Street-Based Sex Workers (SSWs) in Ho Chi Minh City
Sexual Behaviors, Condom Use, and Sexually Transmitted Diseases
The mean number of sexual partners in the prior week was 8.9, including 5.4 casual clients (range, 0–55), 3.2 regular clients (range, 0–28), and 0.3 husbands/lovers (range, 0–3). There was no significant difference between injecting and noninjecting SSWs, except that the injecting SSWs had more casual clients in the prior week (P = 0.002), and a higher proportion of their clients and husband/lovers were drug users (P = 0.001) (Table 2 ). Condom use during the last intercourse was high with casual clients (90.4%), lower with regular clients (78.4%), and much lower with husbands/lovers (42.1%). Condom use was suggested by SSWs during the last intercourse with 78.8% of casual clients, 69.6% of regular clients, and 54.2% of husbands/lovers. Among SSWs who did not use a condom during the last intercourse, objections of casual and regular clients were the main reasons for not using a condom (Table 3 ). Consistent condom use in the prior 12 months was low with casual clients (41.7%), lower with regular clients (40.4%), and very low with husbands/lovers (16.8%). A high proportion of SSWs did not want to use condoms with husbands/lovers and casual clients in the last intercourse (38.5% and 29.6%, respectively). The main reason for not using condoms with their husbands/lovers was the belief that it was not necessary (41.5%).
TABLE 2: Sexual Behaviors of Street-Based Sex Workers (SSWs) in Ho Chi Minh City
TABLE 3: The Reasons for Not Using a Condom During the Last Sexual Act With Different Partners
Having had an STD in the last 12 months was reported by 23.6% (94 of 399) of the SSWs. The SSWs who were younger than 25 years were almost twice as likely to have had an STD in the last 12 months (odds ratio [OR], 1.87; 95% confidence interval [CI], 1.16–3.01). The SSWs who reported anal sex were also more likely to have had an STD in the last 12 months (OR, 2.44; 95% CI, 1.42–4.21). The SSWs who had intercourse during their menstrual period were 3 times more likely to have had an STD in the last 12 months (OR, 3.00; 95% CI, 1.70–5.29). There were several protective factors for preventing STDs, including always using condoms with casual clients in the last 12 months (OR, 0.47; 95% CI, 0.27–0.83) and always using condoms with regular clients in the last 12 months (OR, 0.29; 95% CI, 0.16–0.56).
Intravenous Drug Use
Among the 76 drug users, 51 injected and 25 did not. The mean age of initiating drug use was 22.5 years (range, 14–45 years). The intravenous drug users started injecting at 23.6 years (range, 15–38 years). Among injecting SSWs, 22.4% (11 of 49) had shared needles in the last 6 months, primarily with peers (72.7%) and husbands/lovers (18.2%). Injecting drug SSWs had more casual clients, more regular clients, and more husbands/lovers who injected drugs (P = 0.001) (Table 2 ).
There was a significant association by univariate analysis between intravenous drug use and the following factors: casual clients using drugs (OR, 3.94; 95% CI, 1.61–9.65), regular clients using drugs (OR, 5.04; 95% CI, 2.01–12.66), husbands/lovers using drugs (OR, 7.39; 95% CI, 2.47–22.06), first selling sex before 21 years of age (OR, 3.13; 95% CI, 1.71–5.73), initiating selling of sex for pleasure (OR, 4.79; 95% CI, 1.63–14.08), selling sex because of needing money (OR, 1.93; 95% CI, 1.02–3.66), married before 19 years of age (OR, 2.34; 95% CI, 1.26–4.32), and initiating commercial sex before 19 years of age (OR, 2.61; 95% CI, 1.38–4.96). To determine the independent correlates of intravenous drug use, a multiple logistic regression stepwise analysis was conducted. The result indicated that regular clients using drugs (OR, 3.10; 95% CI, 1.01–9.54), husbands/lovers using drugs (OR, 4.45; 95% CI, 1.29–15.31), first selling sex before 21 years of age (OR, 7.93; 95% CI, 2.97–21.21), initiating selling of sex for pleasure (OR, 10.00; 95% CI, 1.75–57.18), and selling sex because of needing money (OR, 3.06; 95% CI, 1.11–8.46) were independently associated with intravenous drug use.
Knowledge, Perception of HIV/AIDS, and Exposure to HIV/AIDS Prevention Interventions
Among the 361 SSWs who believed that HIV/AIDS could be prevented, 91.7% understood that consistent use of condoms could prevent HIV infection, 57.1% that not sharing syringes and needles could prevent HIV infection, 7.5% that reducing their number of sexual partners could prevent HIV infection, 7.2% that remaining faithful to one faithful partner could prevent HIV infection, and 3.9% that being sexually abstinent could prevent HIV infection.
The perception that they could be infected was highest among those who shared needles and syringes (Table 4 ), ranging from 33.0% to 91.7%. The injecting drug SSWs were more likely to suspect they were HIV-infected (OR, 5.18; 95% CI, 2.74–9.79). The SSWs who had had an STD in the last 12 months also perceived that they were more likely to be infected (OR, 2.16; 95% CI, 1.32–3.55). Access to condoms, needles, leaflets, and peer advice was reported by 58.4% (233 of 399), 15.3% (61 of 399), 44.9% (179 of 399), and 58.4% (233 of 399), respectively.
TABLE 4: Perception of Street-Based Sex Workers That They Could Be Infected
HIV Testing and Risk Factors for HIV Seropositivity
A low proportion (37.0%) of SSWs had been tested for HIV previously. Among HIV-infected SSWs, 40% (26 of 65) had been tested, of whom 61.5% (16 of 26) knew their test results. Approximately 16% (26 of 165) of HIV-positive SSWs reported they did not always use a condom in the last 12 months with casual clients, and 11% (17 of 158) reported no consistent condom use with their regular clients in the last 12 months. Table 5 presents significant associations by univariate analysis between HIV seroprevalence and the following factors: regular clients using drugs (OR, 3.76; 95% CI, 1.52–9.29), husbands/lovers using drugs (OR, 4.16; 95% CI, 1.39–12.42), injecting drugs (OR, 66.15; 95% CI, 28.70–152.44), being younger than 26 years of age (OR, 6.79; 95% CI, 3.78–12.23), being illiterate (OR, 2.04; 95% CI, 1.10–3.78), and initiating commercial sex before 21 years of age (OR, 2.80; 95% CI, 1.63–4.80). To determine the independent correlates of HIV seropositivity, a multiple logistic regression stepwise analysis was conducted. The results indicated that injecting drugs (OR, 101.30; 95% CI, 33.55–305.89) and being younger than 25 years of age (OR, 5.22; 95% CI, 2.10–12.97) were independently associated with HIV seropositivity.
TABLE 5: Univariate Analysis for Correlates of HIV Infection Among Street-Based Sex Workers in Ho Chi Minh City
Discussion
The study population represented a convenience sample of sex workers in the study sites that were locations frequented by sex workers and their clients. It is possible that sex workers not participating were different from those who did participate, but the fact that 94% of sex workers approached agreed to participate in the study suggests that the magnitude of the selection bias was probably low.
SSWs represent a serious potential source or bridge for HIV to spread to the general population of Vietnam. The number of partners reported by SSWs could be high enough to sustain an HIV epidemic. A high proportion (13%) is intravenous drug users, and those who know they are infected continue sex work. Sixteen percent of SSWs in this survey were already HIV-infected. Many of those inject regularly, share injecting equipment, have regular partners or clients who are drug users, have a history of STDs, and infrequently use condoms with both clients and partners. Thus, they demonstrate all the characteristics associated with the rapid spread of HIV from the intravenous drug-using population into the general population, as has occurred in Thailand and Cambodia 12,15 ; but unlike the commercial sex workers in these 2 countries (with the highest rate of HIV in Southeast Asia), a high proportion are also intravenous drug users. It is particularly disturbing that the injecting, street-walking commercial sex workers have more clients than the noninjecting sex workers. Thus, they represent, in many respects, a greater threat to the general population through their clients than the commercial sex workers in either Thailand or Cambodia, the majority of whom do not inject. The unknown is the extent to which Vietnamese males have sex with SSWs and then spread HIV to their wives and other partners. The rate of spread beyond the sex workers will depend on the extent to which men in Vietnam have sex with noncommercial partners, the size of the streetwalking sex worker population, and the proportion of the male population that patronizes SSWs. Thus, there is a need to document the current sexual behavior of males in Vietnam and the existing networks of sexual mixing. A high proportion of truck drivers in Vietnam has been documented by Nguyen et al. 13 to have had multiple partners in the last 6 months.
Multivariate analysis indicated that injecting drugs and young age were associated with a higher risk of HIV infection. Thus, currently, the SSWs are at higher risk because of their drug use than because of their sexual activities. Nonetheless, those who have intravenous drug users as clients and partners are also at risk of sexual transmission from them. The epidemic of intravenous drug use is a relatively new phenomenon in Vietnam, especially among younger men. Thus, older sex workers are less likely to have been exposed to drugs, whereas they were younger than those women currently entering into the sex trade. However, regardless of the source of their HIV infection, SSWs represent a threat to their clients and the future partners of their clients.
The risk factors for injecting among SSWs include partners and clients who inject, selling sex at an early age, needing money from selling sex, and selling sex for enjoyment. Reducing the proportion of SSWs who inject will dramatically reduce the transmission of HIV among them. Thirty-seven percent of the SSWs had been in retraining and detoxification centers. Thus, more effective strategies based on the identified risk factors for initiating intravenous drug use need to be developed.
The literacy rate of SSWs is very low, with 17% being illiterate, meaning that it will be difficult to reach them using media that requires a reasonable level of reading comprehension. Thus, other more direct strategies will need to be implemented. It is also clear that SSWs have very little power to implement safe behaviors on their own. Over 90% were aware that HIV could be prevented, and 92% realized that condoms would reduce their risk; however, condom use was very low. Because of the powerlessness of these women, it will be necessary to also direct intervention messages to their clients and partners. This approach was very successful in Thailand and Cambodia, but in those countries, the majority of commercial sex is conducted through brothels and sex-oriented establishments. Thus, intervention strategies could be directed to the brothel owners, who could be persuaded that if they did not require customers to use condoms, they could be closed. 16 SSWs work independently, not in establishments; thus, it is necessary to direct intervention strategies to them and their clients, a much less efficient and effective strategy for effecting behavior change. Innovative strategies to reach these SSWs and their partners will need to be implemented. The strategy must target both intravenous drug use and the need for condoms.
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