SEXUALLY TRANSMITTED INFECTIONS (STIs), including HIV infection, may be spread from high-prevalence or “core” populations to low-prevalence populations through drug users who engage in heterosexual activities with their spouses or with other regular sex partners.1,2 In this way, drug users serve as a bridge population between the core group and the general population. Drug users who share needles and engage in sex with both high-risk partners such as commercial sex partners and low-risk partners such as their spouses or regular sex partners are defined as a bridge population.3 In addition, drug users who become HIV-infected by sharing contaminated needles or equipment may spread the virus to their wives or regular sex partners through unprotected sex.4,5
The sexually transmitted disease (STD) and HIV epidemics in China are growing rapidly.6,7 Drug use, especially intravenous drug use, is widespread in China and is a major source of the rapidly expanding HIV epidemic.8 Although HIV infections through all transmission routes are increasing in absolute numbers, the majority of new HIV infections (66.5% of reported HIV cases) are still attributed to injecting drug users (IDUs).9 It has recently been reported that the HIV/AIDS epidemic is spreading into the general population.8 However, precisely how HIV is transmitted throughout the general population in China remains unclear. There is evidence that the proportion of sexually transmitted HIV infections is increasing. Data from China’s national surveillance sites document that the proportion of female HIV cases has increased considerably in recent years.10 Sexual spread of STI/HIV from IDUs to their sex partners and children has been documented in two of China’s neighboring countries, Thailand11 and India.12 Most research studies of IDUs in China have focused on HIV-related risks.13–15 Few have investigated drug users as a bridge population sexually transmitting STIs, including HIV, to their partners. To better understand HIV-related risks in both bridge and nonbridge populations, we conducted a study among drug users in Anhui province, which examined both their risk characteristics and their sexual mixing patterns in the heterosexual population.
Materials and Methods
Study Sites and Subjects
This study was conducted in Anhui Province. Anhui is located in Eastern China, with a population of 62.3 million, where 83% of the population is rural. The first AIDS case in Anhui was reported in December 1994. From 1994 to 2004, 2,068 HIV cases were reported from 16 cities and 54 counties in the province. Anhui ranks seventh in HIV prevalence among the 31 Chinese provinces.16 The infection rate continues to accelerate in Anhui with 401 cases reported in 2002 and 967 cases in 2003, reflecting a 2.4-fold increase. The majority of HIV cases are among farmers (95.3%) and former blood plasma donors (85%).
Anhui is facing another serious epidemic: illicit drug use. According to the China Anti-Drug Yearly Report in 1999,17 Anhui was identified as one of 11 provinces with a drug-related crisis. A report from HIV sentinel surveillance in Anhui shows that the prevalence of HIV among drug users was 1.2% in 2003.18 In Hefei, the capital of Anhui province, there are three drug detoxification centers, two for male drug users and one for females. In 2003, 713 drug users received detoxification treatment in the three centers. The female detoxification center and one male detoxification center were selected as study sites. The smaller male detoxification center was excluded because of its size and because most of the drug users were considered criminals. Drug users stayed in the two centers receiving either voluntary or compulsory drug treatment for an average period of 5 months. All drug users in the two selected centers were eligible for participation. Study protocols were approved by the UCLA General Campus Institutional Review Board and the Hefei Centers for Disease Control and Prevention.
A structured questionnaire without personal identification information was administered to subjects. Subjects were informed that the study was voluntary, that their identity would be kept confidential, and that they would not incur any negative consequences for nonparticipation. Staff from the detoxification centers, except the medical doctor, did not participate in the study. The questionnaire was piloted with five drug users and changes were made as needed. After signed informed consent, each participant completed a face-to-face interview. Trained interviewers were paired with subjects of the same gender. Participants were interviewed in a private room in each center.
Knowledge regarding transmission and prevention of HIV/AIDS was measured by 13 true/false (unknown) questions. One point was awarded for each correct answer with a possible score ranging from zero to 13 points.
Perceived Vulnerability to HIV Infection.
Perceived vulnerability was measured by the following question: “People have different ideas about their risk of getting HIV/AIDS. What do you think the chances are that you will acquire HIV?” Response choices were: (1) it almost certainly will not happen, (2) it could happen, (3) it probably will happen, or (4) it almost certainly will happen. A binary variable was created by combining 2, 3, and 4.
Sex partners were defined into two categories, regular sex partners and commercial sex partners. Regular sex partners included spouse and partners who lived with respondents who did not ask for financial compensation or exchange sex for drugs. Commercial sex partners were defined as those who sold or bought sex or exchanged sex for drugs.
Bridgers and Nonbridgers.
Bridgers were defined as participants (1) who had both regular and commercial sex partners in the past year; and (2) who shared needles with others and had sex with regular sex partners. Participants who had only regular sex partners or had no sex in the past year were defined as nonbridgers.
Participants were tested for HIV-1, hepatitis C virus (HCV), and syphilis. For primary screening, all serum samples were tested for HIV-1 antibodies by commercial enzyme-linked immunoassay (ELISA; HIV Uni-form II plus O; Wantai Biologic Medicine Co., Beijing, China). Reactive (positive) samples were confirmed with Western blot (WB; HIV Blot 2.2 WB; Genelabs Diagnostics, Singapore). The enzyme immunoassay (EIA) for testing HCV antibody was used (HCV test kit; Shiyekehua Biotec Inc., Shanghai, China). Positive samples were retested. The toluidine red unheated serum test (TRUST) was used for screening testing for syphilis (TRUST test kit; Rongsheng Biotec Inc., Shanghai, China. For Treponema pallidum, the particle agglutination test (TP-PA) was used for confirmation (SERODIA; Fujirebio Inc., Tokyo, Japan).
Two research assistants independently entered the data into a computerized database using Epi-Info 6.12 (Centers for Disease Control and Prevention, Atlanta, GA). Bivariate analyses (Student t test or χ2 test) and multiple logistic regression analysis were performed to estimate the crude odds ratios (cORs), adjusted ORs (aOR), and their 95% confidence intervals (CIs) of injection and sexual risk behaviors associated with the bridgers using SAS 9.1 (SAS Institute, Cary, NC).
Description of the Study Population
All of the 312 drug users in the two centers were invited and agreed to participate in the study. More than 60% (61.2%) were men. The mean age of participants was 27.9 (standard deviation [SD] = 6.48). Almost 70% (69.6%) had an educational level higher than primary school. Approximately two thirds (68.6%) were unmarried; 72.4% of the subjects (226) ever injected drugs; 18.9% (59) shared needles and syringes with others in the past 30 days; 39.7% (124) of the drug users reported having both regular and commercial partners in the past year and; 47.8% reporting having only regular sex partners. Table 1 presents descriptive statistics of the study population stratified by gender. Male drug users were approximately 2 years older than females. Female drug users initiated drug use 2 years earlier than males. Approximately half (49%) of the female drug users worked in entertainment venues, whereas half of the males did not have a job in the past 6 months. More female than male drug users shared needles and syringes in the past month and had more regular and commercial sex partners in the past 12 months. Although drug users were relatively well informed about HIV/AIDS, they did not perceive themselves at high risk.
Demographic Characteristics of Bridgers and Nonbridgers
A substantial number of drug users were bridgers (49.4%; N = 154). Compared with nonbridgers, bridgers were on average younger, unmarried, female, had a higher education level, or worked in entertainment venues (Table 2).
Injection and Sexual Risk Behaviors Among Bridgers and Nonbridgers
Among bridgers, 83.1% injected drugs; 76.6% (118 of 154) injected drugs two or more times per day; and 35% (54) shared needles or syringes with others in the past month before they entered the centers. Among nonbridgers, 62% injected drugs; 48.7% (77 of 158) injected drugs two or more times per day; and 3.2% (5) shared needles or syringes. Eighty-seven percent (134) of bridgers and none of nonbridgers reported having one or more commercial sex partners in the past year. Condom use with regular sex partners was extremely low among both bridgers and nonbridgers. Only 3.9% of the bridgers and 4.6% of nonbridgers used condoms every time or almost every time. More bridgers (33%) than nonbridgers (18%) perceived risk of HIV infections. There was no difference on HIV/AIDS knowledge between the two groups. Adjusted for age, gender, education, occupation, and marriage status, multiple logistic regression analysis showed that bridgers compared with nonbridgers more frequently injected drugs, had more injecting partners to share their needles and syringes, had more regular sex partners, and perceived themselves to be at risk of HIV infection (Table 3).
HIV Infection, Syphilis, and Hepatitis C Virus Infection Among Bridgers and Nonbridgers
Only one study participant (a male bridger) tested positive for HIV infection. Fifty-eight percent (90 of 154) of bridgers and 46.8% (74 of 158) of nonbridgers tested positive for HCV (χ2 = 4.21, P = 0.04). Twenty-four (15.6%) bridgers and 11 (7%) nonbridgers tested positive for syphilis ((χ2 = 5.82, P = 0.02). Eighteen (11.7%) bridgers and 25 (15.8%) nonbridgers reported having previously received an HIV test (χ2 = 1.12, P = 0.29).
Sex Partners, Condom Use, and Needle Sharing Among Male and Female Bridgers
Forty-seven percent (34 of 73) of male bridgers and 74% (60 of 81) of female bridgers reported having three or more commercial sex partners in the past year. More than half (53.5%) of female bridgers and only 8.2% of male bridgers used condoms every time or almost every time with their commercial sex partners. Eighty-two percent of female bridgers sold sex in the past month and the majority of male bridgers (58.9%) bought sex or exchanged sex for drugs in the past month before they entered the centers. Forty-nine percent (36 of 73) of male bridgers and 37% (30 of 81) of female bridgers had two or more regular sex partners in the past year. However, only 1.5% of male bridgers and 6.5% of female bridgers reported using condoms every time or almost every time with their regular sex partners (Table 4). The frequency of sharing needles or syringes was similar among male and female bridgers. One male bridger reported having a male sex partner.
To the best of our knowledge, this is the first study in China to document and compare risks for STDs, including sexually transmitted AIDS, between a bridge population and a nonbridge population. The STD-related risks and sexual mixing patterns found in the bridge population raise the possibility that a general epidemic of STDs and AIDS in China may be promoted by drug users.
Bridgers’ sexual behavior may fuel the spread of STIs into the general population.19 Transmission potentiality is influenced directly by (1) the prevalence of STI/HIV infection in the core population, (2) the frequency of unprotected sex among bridgers, and (2) the density of bridgers. The high prevalence of STIs, including HIV infection, among drug users and commercial sex workers has been repeatedly documented in China.14,15,20 The relative high prevalence of syphilis (15.6%) among the bridgers in this study suggests that bridgers are capable of transmitting STIs to their spouses and their regular sex partners. Although HCV prevalence was fairly high, HIV prevalence in this study was low. In comparison, HIV prevalence among IDUs in Yunnan, Guangxi, and Sichuan province was between 11% and 77%.15,21 The main reason for low HIV prevalence among drug users in Anhui is that the major HIV transmission route in the province is commercial blood donation and only a limited number of the donors can financially afford to use drugs.22,23 As a result of limited funds, we only tested for syphilis, not for gonorrhea or chlamydia. One study of sex workers in China reported that the prevalence of chlamydia, gonorrhea, and syphilis were 32.2%, 8.8%, and 5.4%, respectively.24
We found that unprotected sex among bridgers was common. Half the female bridgers and 8% of male bridgers used condoms consistently with their commercial sex partners. Even more alarming was the finding that only 1.5% of male and 6.4% of female bridgers used condoms consistently with their regular sex partners. The low rate of condom use with regular sex partners implies that there may be a significant impact on STI transmission through bridgers.
It is significant that the percentage of bridgers in this study was high (49.4%) and similar to the percentage of bridgers (40%) that was found in a study of sex worker clients in Cambodia.25 This percentage is higher than that found in two other studies of bridgers, one in Thailand (17% of men and 25% of truckers)26 and one in Cambodia (20.5% of military personnel, 15.7% of police, and 14.7% of motorcycle drivers).27 The majority of female drug users worked in entertainment venues. Because prostitution is still illegal in China, entertainment venues are underground brothels.28 According a recent report, 80% of female drug users in China sold sex for exchanging drugs.29 In our study, 81.5% of female bridgers sold sex in the past 30 days. In light of the apparent marked growth of both the drug user population and the commercial sex worker population in China,9 the high density of bridgers is likely to contribute to the rapid spread of the STI/HIV epidemics from populations engaging in higher-risk behaviors to those engaging in lower-risk behaviors.
According to the assortative/disassortative mixing model, some optimal combination of assortative and disassortative mixing is associated with the rapid, generalized spread of STI/HIV.30,31 The importance of disassortative mixing is that it provides a bridge of infection from one population to another.32 Drug users in the current study had properties of both assortative and disassortative mixing partners. Bridgers as compared with nonbridgers had a higher level of drug-related risks for HIV infection; a higher frequency of injecting drugs; and more injecting partners with whom they shared needles and syringes. Thus, their assortative mixing properties placed them at risk in the acquisition and transmission of HIV within the drug users’ own community. At the same time, because many drug users had both higher-risk and lower-risk sex partners, they also have the property of disassortative sexual mixing, which may facilitate sexual transmission of STI/HIV into the low-risk population because few drug users share needles and syringes with their partners.
Although HIV/AIDS knowledge was relatively high among drug users, this group did not perceive themselves to be at risk of HIV infection and very few had received an HIV test. Lacking awareness of HIV infection status, drug users may continue to practice risky behaviors with their sex and/or drug-use partners. The low condom use among drug users reflects this continuation. Several studies conducted in China have revealed that over 90% of detoxified drug users relapse.33,34 It is likely therefore that many drug users once released from a detoxification center will return to unsafe injection behaviors and unprotected sex. Thus, it is crucial to educate through counseling both HIV infected and noninfected drug users so they may adopt and maintain safer behaviors. Because HIV voluntary counseling and testing (VCT) has been shown to be effective with regard to both STI and HIV control and prevention in developing countries,35 an organizationally based VCT intervention program targeting reducing STI/HIV transmission resulted from both assortative and disassortative mixing partners needs to be implemented more widely in detoxification centers in China.
This study has several limitations. First, the study findings from only two detoxification centers may not be generalizable to other centers in China. Systematic study of bridgers and nonbridgers situated in other provinces in China with large numbers of drug users are needed. Second, as a result of the cross-sectional nature of this study, study data should be interpreted as associations and does not imply causality. Third, because sexual risk behaviors are not socially accepted in China, it is possible that participants may have provided socially desirable responses and underreported multiple sex partners and unprotected sex. Thus, the results may be conservative. Fourth, because only syphilis was tested among drug users, the true number of drug users infected with STDs may be underestimated.
Despite these limitations, the findings provide potentially valuable and useful information on STI/HIV-related risks among drug users and their bridging role in spreading the STI/HIV epidemic. Systematic study of bridgers and nonbridgers situated in other provinces in China with large numbers of drug users are needed. If the findings of the current study are robust, intervention efforts should be considered to prevent STI/HIV infection within the drug users’ community and reduce transmission to the general population. China has recently started methadone maintenance treatment of drug users and clean needle exchange programs.10 Promotion of safer sex should be integrated with these and other harm reduction programs.
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