Related epidemics of injection drug use and HIV/AIDS have been documented in more than 100 countries on every continent.1 Cross-border areas, such as that encompassing Lang Son Province in northern Vietnam and Guangxi Province in southern China, offer unique but challenging opportunities for addressing these dual epidemics. Beyrer and colleagues2 described a heroin transshipment route leading from the Golden Triangle of Thailand, Myanmar, and Laos, a leading heroin-producing region, into northern provinces of Vietnam; thence into Guangxi Province, China, to Nanning, the provincial capital; and finally to Hong Kong and the rest of the world. With the increasing availability of heroin along this transshipment route, opium smoking gave way to smoking and inhalation of heroin and often to heroin injection, largely because of the cost-effectiveness of this method. Most heroin injectors are poor people who often cannot afford new needles and syringes despite their widespread and inexpensive availability in pharmacies or cannot access pharmacies at night when they need to obtain needles. These circumstances resulted in sharing of injection equipment and transmission of HIV.3-8
HIV prevalence among injection drug users (IDUs) in southern China is highest in Yunnan Province to the west of Guangxi, where HIV prevalence among IDUs in some localities is about 75%.9 The epidemic in Guangxi has not yet reached these proportions.10 In Ning Ming County, the initial survey of IDUs reported in this article revealed an HIV prevalence of 17%. In Vietnam, HIV prevalence among IDUs has reached 65% to 74% in some northern provinces,11-14 whereas in Lang Son, our initial survey revealed a 46% prevalence.
Molecular epidemiologic findings are consistent with the hypothesis that HIV has spread across the border from northern Vietnam into southern China.2,15-19 Beyrer and colleagues2 identified matching strains of subtype E on both sides of the border, a strain hitherto commonly found in Vietnam but not in other parts of China, including Yunnan, where subtype C predominates. Genetic analysis by Kato et al19 of 24 blood samples collected in Lang Son and Quang Ninh Provinces from 1998 to 1999 concludes that a highly homogeneous variant of HIV subtype E is present in Lang Son and across the border in Pingxiang, Guangxi Province, China. These findings suggest that cross-border HIV transmission could have occurred in either or both directions between northern Vietnam and southern China.
The HIV epidemic in northern Vietnam and southern China is fuelled by complex patterns of small-scale cross-border movement of drug dealers and drug users. The 200-km border between Guangxi and Vietnam is largely mountainous and remote. There is only 1 official crossing and about 5 “semiofficial” crossings, where one can pay a small fee to cross. Otherwise, the border is essentially open. During site visits, we observed hundreds of people crossing in both directions at semiofficial gates in the course of a half hour with no supervision or control. Drug users and dealers reportedly cross the border, but the patterns are variable and are influenced by the current price and purity of heroin, the ebb and flow of law enforcement activity, and, more recently, the outbreak of severe acute respiratory syndrome (SARS).
There is also substantial legitimate trade and migratory employment in the region. Lang Son City, Aidian, and Puzhai (near Pingxiang) are bustling centers of legitimate cross-border trade as well as drug trafficking and sex work. Many people cross the border daily and seasonally to find work, and many are employed as porters in the cross-border trade. The region is home to many ethnic minority groups (eg, Zhuang, Tay, Nung), some of whom live on both sides of the border. The Zhuang in China and the Tay in Vietnam are the same ethnic group, related to Thais, but have different names in the 2 countries. There is frequent intermarriage across the border, and kinship ties, like migratory employment and trade, result in additional cross-border movement.
With support from the National Institute on Drug Abuse (NIDA) and the Ford Foundation, we implemented a 4-year HIV prevention intervention in 2002 for IDUs at 6 sites in Lang Son Province, Vietnam, and 4 sites in Ning Ming County, Guangxi Province, China. This is the first cross-border HIV prevention project targeting IDUs in which the same interventions are being implemented in both countries. Figure 1 shows the geographic setting of the project and locates the sites. At each site, salaried peer educators, most of whom are active heroin injectors, contact other IDUs in the community, provide HIV risk reduction information, distribute new needles/syringes and vouchers good for new needles/syringes and other risk reduction supplies at participating pharmacies, and collect and dispose of used needles/syringes.20,21
The intervention aims to reduce HIV risk behaviors among IDUs and thereby stabilize HIV prevalence and reduce HIV incidence on both sides of the border as well as to prevent cross-border HIV transmission. We consider this a structural intervention because it seeks not only to influence the behavior of individual IDUs but also to diffuse HIV risk reduction messages and sterile injection equipment through the IDU community.22 Thus, we expect that HIV information and safer injection materials will reach IDUs who do not personally participate in the intervention. We also hope to diffuse knowledge of HIV and inculcate support for the intervention throughout the general community and to benefit the larger public health by collecting and disposing of large numbers of discarded needles and syringes that might otherwise put children and other members of the community at risk. The project involves intensive community education and regular meetings with relevant agencies, including the police, to increase awareness of HIV/AIDS and to build support for the intervention.
A structural intervention such as this is appropriately evaluated at the community level. Thus, the evaluation relies on cross-sectional surveys of IDUs (including interviews and HIV testing) just before the start of the interventions and at 6-month intervals after implementation. This is not a cohort study, but some IDUs likely participate in multiple cross-sectional surveys, and their records are linked by means of unique participant identification numbers. This article reports on the relations among border-related factors, drug-using and sexual behaviors, demographic characteristics, and HIV status among the samples of IDUs in the cross-sectional survey conducted just before the interventions were initiated.
Data collection methods were parallel in Ning Ming County and Lang Son Province, with some variation in the subject recruitment strategies used. To be eligible, a participant had to be at least 18 years of age and to have injected heroin in the past 6 months.
In Ning Ming County, a modified “snowball/peer recruitment” technique was used. The project peer educators sent letters to IDUs they knew personally, inviting them to come to participate in the survey. The IDUs who came to project centers for interviews were encouraged to recruit 2 to 3 additional participants. The research participants received 20 Chinese yuan (approximately $2.50) for the interview, 5 yuan for each additional male respondent recruited, and 10 yuan for each additional female respondent recruited.
In Vietnam, approximately half of the sample was based on lists of registered IDUs in the project sites and the other half was based on individuals selected from IDUs present at gathering or shooting places mapped by the study team. For the half of the sample based initially on registered lists, 10 clusters of 25 individuals each were selected with probability proportional to size (PPS) from the lists of IDUs in each commune. Four IDUs were then picked at random from each selected cluster, and these individuals referred others, and so on, by the snowball method until the quota for the commune was reached. For the portion of the sample selected initially at IDUs' gathering or shooting places, sample quotas were determined by PPS based on the numbers of individuals observed at these places during the mapping phase. The interview team then visited the selected places and chose 4 individuals at random from among those present at each place at that time. The quotas for each place were then filled by the snowball method. The Vietnamese participants were paid 30,000 dong (approximately $2.00) for the interview and HIV test.
In Vietnam, oral informed consent was obtained from participants, with the interviewer certifying that oral consent by signing the form. This procedure was recommended by the Institutional Review Board of the National AIDS Standing Bureau to provide more assurance of confidentiality to prospective participants. In China, standard signed informed consents were obtained from all participants. Unique codes were constructed for each participant based on the numeric date of birth and several letters representing, for example, the first letter of the mother's family name. Construction of the record number was slightly different in the 2 countries. The objective was to have a unique identifier composed of items that participants could readily remember to obtain their HIV test results. Results were coded only by these identifiers.
A structured instrument was used for the interviews based on version 2b of the questionnaire being employed in the World Health Organization's Drug Injection Study, phase 2.23 The interviews were conducted by trained interviewers, primarily staff of the local health departments. The first cross-sectional surveys were conducted in July 2002 in Vietnam and between July and September 2002 in China. Data sets were prepared in EpiInfo, version 6.04, by staff of the Guangxi Center for HIV/AIDS Prevention and Control and the National AIDS Standing Bureau of Vietnam; the latter subsequently merged into the General Department of Preventive Medicine and HIV/AIDS Control of the Ministry of Health. The data were analyzed at Abt Associates using SAS, version 8.2 (SAS, Cary, NC).
The survey included HIV antibody testing. Participants were given pretest counseling and posttest counseling at local health centers. Blood was drawn at the time of the interviews by trained phlebotomists from local health departments. Participants were given a card with their unique identifier and told that they could return on a certain date to the local health center to receive their test results using this number.
In China, testing was by double enzyme-linked immunoassay (ELISA, Vironostika HIV-uniform; Organon, Holland), with confirmation of initial HIV-positive results by Western blot methodology (Genelabs Diagnostics). All testing was conducted at the laboratory of the Guangxi Center for HIV/AIDS Prevention and Control in Nanning. In Vietnam, testing was performed at the laboratory of the Lang Son Provincial Health Services by means of the Serodia SFD screening test (Biorad, France) and double ELISA (Genescreen, Biorad; Vironostika, Organon). This is the official protocol of the Ministry of Health in Vietnam.
The study was reviewed and approved by the institutional review boards (IRBs) of the following institutions: Guangxi Center for HIV/AIDS Prevention and Control, the National AIDS Standing Bureau of Vietnam, Abt Associates, and Beth Israel Medical Center.
In addition to HIV positivity determined through testing as described previously, a series of demographic, knowledge, and self-reported behavioral variables from the cross-sectional IDU surveys were used in this analysis. Most of the behavioral variables are based on questions about specific drug-, sex-, and border-related activities during the 6-month period before the interview.
We prepared descriptive statistics on the demographic characteristics and HIV and hepatitis knowledge of the samples of IDUs. Correlates of HIV status were explored through bivariate and multivariate analyses. Variables with some apparent statistical relation to HIV status in bivariate analyses (in most cases, P values of 0.10 or lower using a Wald test based on a logistic model) were then assigned to 3 groups of related variables (demographic, border-related, and knowledge- and risk behavior-related) for multivariate logistic regression analysis. The analysis was first done by variable groups to assess which, if any, of these groups as a whole seemed to be related to HIV status. After this, additional logistic models were run to identify significant predictors within the selected groups.
Table 1 summarizes key characteristics of the samples of IDUs in Lang Son and Ning Ming. Both samples were overwhelmingly male, and most IDUs were aged 21 to 30 years. There are known to be female IDUs at these sites, and 29 (10%) of the participants in Ning Ming were women, where the project has several female peer educators. Only 2 (<1%) of the respondents in Lang Son were women. Female IDUs are a particularly stigmatized and hidden population in Vietnam and China and are thus extremely hard to reach with interventions and research activities. Female IDUs reportedly tend to inject at home or in private rather than in groups or at shooting places. They may also inject with their male sexual partners. In behavioral surveillance surveys carried out in several Vietnamese provinces, the samples of IDUs were entirely male.5 Indeed, it is as if Vietnamese IDUs are considered male by definition, whereas the only women who inject drugs are presumptively categorized as sex workers.
The samples of IDUs in both countries were predominantly single, and most of them had never been married. About 75% of the participants in China and more than 50% in Vietnam were members of ethnic minority groups. Previous HIV testing was much more common among the IDUs in Vietnam than in China, and the HIV prevalence was much higher in Lang Son (46%) than in Ning Ming (17%). The patterns of HIV prevalence among IDUs at the project sites are described elsewhere (Des Jarlais DC, Johnston P, Friedmann P, et al. Patterns of HIV prevalence among injecting drug users in the cross-border area of Lang Son Province, Vietnam and Ning Ming County, Guangxi Province, China. (Submitted for publication)).
Analysis of the HIV and hepatitis knowledge test questions, shown in Table 2, revealed that IDUs in Lang Son Province, Vietnam, are generally more knowledgeable about the means of HIV transmission than their counterparts in Ning Ming County, China, although there were substantial knowledge deficits in both countries. Only about 50% of the IDUs in Ning Ming knew that HIV can be transmitted through needle sharing, and slightly more than 25% knew that HIV can be transmitted through unprotected sex. Less than 25% of respondents in both countries were aware that HIV can be transmitted through sharing of other injection equipment. Thirty percent of the Chinese IDUs did not know any ways in which HIV is transmitted. Average scores on a composite variable that summed correct answers on 3 key HIV transmission routes (needle sharing, sexual intercourse, and blood-to-blood contact) on a scale of 0 to 3 were higher among IDUs in Vietnam than among those in China (2.6 vs. 1.6; P < 0.0001). In Vietnam and China, levels of HIV knowledge were higher among HIV-positive IDUs than among those who were HIV-negative, and the difference was statistically significant in Vietnam (P = 0.030).
More of the IDUs in China than in Vietnam had heard of hepatitis, but less than 20% in both countries were aware that hepatitis infection can be spread through needle sharing; in fact, more than 50% knew no ways that hepatitis is transmitted.
Table 3 lists possible demographic, knowledge- and risk behavior-related and border-related correlates of HIV status among the IDU samples. Three quarters of the IDUs in China and about half in Vietnam reported some sharing of injection equipment in the past 6 months. Self-reported rates of receptive and distributive sharing of needles/syringes in Vietnam were low, however, with about half of Chinese IDUs reporting these behaviors. Self-reported cross-border purchasing of drugs was surprisingly infrequent among IDUs in both countries.
About half of the respondents in both countries were heterosexually active, and small percentages (smaller in Vietnam) reported recent unprotected intercourse with a casual partner or payment for sex during the previous 6 months.
Tables 4 and 5 report bivariate and multivariate analyses by logistic regression of the correlates of HIV status among IDUs at the sites in Ning Ming County, China. The bivariate analyses (see Table 4) reveal some predictable relations among border-related and drug-using behaviors and HIV status. For example, purchase and injection of drugs by Chinese IDUs across the border in Vietnam (where the background prevalence among IDUs is substantially higher) during the last 6 months were related to HIV positivity, as was a composite variable reflecting the interaction of sharing injection equipment and obtaining needles/syringes from potentially unsafe sources. Ethnic minority status and living closer to the border were also related to HIV positivity, and being older was related to HIV negativity. In the logistic regression analysis for China by variable groups, the border-related and demographic groups emerged as potential predictors of HIV status, whereas the knowledge- and risk behavior-related group fell out.
The results of the logistic regression analysis for the variables in the surviving groups, reported in Table 5, show that only living closer to the border, greater frequency of buying drugs across the border, and younger age emerged as statistically significant predictors of HIV positivity at the Chinese sites. Subsequent analysis gave no indication of binomial overdispersion.
In Vietnam, a different pattern emerged. Bivariate analysis (Table 6) showed that only 2 drug-related risk behaviors were predictably related to being HIV-positive, a composite variable reflecting intensity of injecting (years injecting × frequency of injection) and sharing injection equipment with an HIV-positive person, whereas 3 others (frequency of buying drugs across the border, the composite variables reflecting sharing injection equipment, and the interaction of sharing injection equipment with obtaining needles/syringes from potentially unsafe sources) seemed to be anomalously related to HIV status; that is, higher risk behavior was related to being HIV-negative, and taking risk reduction measures was related to being HIV-positive. Additionally, greater HIV knowledge was related to being HIV-positive, and being married or living as married was related to HIV negativity. Sexual risk behavior was not related to HIV status among the Vietnamese IDUs.
Logistic regression analysis by variable groups for Vietnam resulted in the survival of all 3 groups. Further analysis of individual variables in the 3 groups (Table 7) showed that the composite variable reflecting interaction of sharing injection equipment and obtaining needles in unsafe places retained its apparently anomalous relation to HIV-positive status; that is, the lower the riskiness of behavior, the greater the likelihood of being HIV-positive. Higher levels of HIV knowledge also remained statistically related to HIV positivity. Conversely, in Vietnam, sharing injection equipment with an HIV-positive person remained predictably related to HIV positivity. Living farther from the border was related to HIV positivity, and frequency of buying drugs across the border was related to HIV negativity.
In China (P = 0.01) and Vietnam (P = 0.14), higher levels of HIV knowledge were predictably related to HIV risk reduction behavior (ie, obtaining needles in “safe” places, reducing or discontinuing the sharing of injection equipment). In Vietnam, 98% of HIV-positive IDUs reported taking some steps to reduce their risk of acquiring or transmitting HIV since hearing about HIV, whereas 62% of HIV-positive IDUs in China reported taking some risk reduction measures (the respondents did not necessarily know their HIV status at the time of the interview). The relation between HIV-positive status and engaging in any risk reduction measure was close to being statistically significant in Vietnam (odds ratio [OR] = 6.18; P = 0.090) but not in China (OR = 0.96; P = 0.897).
This analysis of the correlates of HIV status suggests some differences in these patterns between China and Vietnam. In China, border-related factors (living closer to the border and buying drugs across the border) as well as younger age were the strongest predictors of HIV positivity. Although relatively few Ning Ming IDUs reported crossing the border, this behavior seems to be particularly risky, and its effect may have been amplified as border-crossing IDUs who acquired HIV in Vietnam returned to Ning Ming and transmitted HIV to additional injectors who had never themselves crossed the border.
In Vietnam, by contrast, there were some apparently anomalous relations whereby less sharing of injection equipment and obtaining more needles from safe sources were associated with HIV positivity. Levels of HIV knowledge were also higher among HIV-positive IDUs in Vietnam than in China, suggesting a link between knowledge and behavior.
Thus, border-related factors rather than other behavioral risks are the strongest predictors of HIV status in China, whereas HIV status (and HIV knowledge) seems to drive behavior in Vietnam. This interpretation is consistent with a “gradient” pattern of HIV prevalence at project sites across the 2 countries, which we report elsewhere (Des Jarlais DC, Johnston P, Friedmann P, et al. Patterns of HIV prevalence among injecting drug users in the cross-border area of Lang Son Province, Vietnam and Ning Ming County, Guangxi Province, China. (Submitted for publication)) indicating that heroin injection and HIV infection may have begun earlier on the Vietnamese side of the border and that there has been cross-border transmission of HIV from Vietnam into China.2 Also consistent with this finding are the facts that IDUs in China have begun injecting more recently than those in Vietnam and that IDUs in Vietnam are more knowledgeable about HIV. Having a longer self-reported injection history was related to being HIV-positive in Vietnam (OR = 1.06; P = 0.07) but not in China (OR = 0.998; P = 0.97). Also, in Vietnam, having a previous HIV test was strongly related to being HIV-positive (OR = 3.326; P < 0.0001), but this relation did not hold in China, where far fewer participants had been tested before (OR = 0.826; P = 0.767).
In other words, in Lang Son, the intertwined epidemics of heroin injection and HIV probably began earlier; thus, HIV prevalence and HIV knowledge have reached significantly higher levels there than found just across the border in Ning Ming. One might expect that this sequence of events would begin simultaneously all along the heroin transshipment route. Instead, these developments seem to have moved gradually from south to north along the route. As a result of the earlier onset in Lang Son, more IDUs there are HIV-positive and may be reacting behaviorally to being HIV-positive. Their greater likelihood of engaging in risk reduction measures may reflect some combination of a belief that they can avoid “reinfection” or deterioration of their medical condition if they reduce their risk behaviors and an altruistic desire to avoid infecting others.
It is possible that the different sample recruitment methods used for the cross-sectional IDU surveys in China and Vietnam account for the differential HIV prevalences found in the 2 countries. In particular, the partial reliance of the Vietnam sample on lists of registered IDUs may overstate HIV prevalence compared with an IDU sample based entirely on snowball methods as used in China. Prevalence figures for IDUs at some nearby sites in China and Vietnam reveal a similar differential, however. In Hanoi (about 150 km from Lang Son) and Bac Ninh (about 100 km away from Lang Son), Vietnam, HIV prevalence among IDUs is similar to that found in our surveys in Lang Son-40% to 45%.24,25 Likewise, HIV prevalence among IDUs in Pingxiang, Guangxi (about 50 km from Ning Ming), is similar to that found in Ning Ming-about 22%.10
Data from follow-up surveys should reveal whether the cross-border patterns of HIV prevalence among IDUs found before the start of the interventions remain stable within limits of random variation or reflect increases below what might have been expected in the absence of the interventions. If we observe stability of prevalence and low HIV incidence, we believe we can reasonably conclude that our interventions have been successful in controlling cross-border and intracountry HIV transmission. These follow-up data should also show whether the differing relations between behavior and HIV status identified before the start of the interventions in the 2 countries are maintained as implementation continues over longer periods and as the epidemics of heroin injection and HIV become more mature.
The authors gratefully acknowledge all the health department and clinic staff, other public officials, peer educators, and pharmacists in Ning Ming County and Lang Son Province who are participating in and supporting this project. They also acknowledge the support and encouragement of Lisa Messer-smith of the Ford Foundation's Hanoi office, Joan Kaufman and Eve Lee of the Ford Foundation's Beijing office, and Helen Cesari of the NIDA, US National Institutes of Health.
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