Abstract
This study aimed at understanding the HIV prevalence, distribution of HIV risk factors and whether the HIV has spread from high-risk groups to the general population in the Yanyuan and Muli counties, Liangshan Prefecture, Sichuan Province, China. A multistage probability method was used to select a representative sample of villages in each county, with stratification by risk employed in the sampling for the Yanyuan county. A real-name registration and confidential method were adopted to collect the information of the participants. Blood specimens were tested for HIV, syphilis, and hepatitis C virus. A total of 4,950 subjects participated in the study. Of the participants aged ≥ 15 years, 0.12% self-reported being drug users and 40% were injection drug users; 0.46% had multiple sex partners and the condom use rate was only 26.3% during the last sexual intercourse. HIV, syphilis, and HCV prevalence of Yanyuan county were 0.06% (95% CI: 0–0.142), 0.06% (95% CI: 0–0.142), and 0.15% (95% CI: 0.020–0.280), respectively. HCV prevalence of Muli county was 0.06% (95% CI: 0–0.191), and none was found to be HIV or syphilis positive. Therefore, the rate of HIV infection in Yanyuan and Muli counties is at a low level currently. The Yanyuan county HIV infection rate is similar to the average rate in all of China, and the Muli county rate is below China's average. The HIV epidemic has not spread from high-risk groups to the general population in these two counties. J. Med. Virol. 84:1–5, 2011. © 2011 Wiley Periodicals, Inc.
INTRODUCTION
Liangshan Prefecture in Sichuan Province, China, which has 1 county-level city and 16 counties, with a population of 4.61 million persons, is located along one of the main drug trafficking routes from the “Golden Triangle” to northwest and central China, one of the largest illicit drug (especially heroin) production and distribution centers of China [Ruan et al., 2004, 2005; Sichuan Provincial CDC, 2008; Liangshan Prefecture CDC, 2008]. The first person infected with HIV was identified in Dehong Prefecture, Yunnan Province in 1989, and since then HIV infection has spread along drug trafficking routes to injection drug users in nearby cities, including the Liangshan Prefecture [Wu, 1999; Lu et al., 2004; Xiao et al., 2007]. By the end of June 2009, the cumulative number of persons infected with HIV reported in the Liangshan Prefecture was 15,700, including 528 AIDS cases and 700 deaths. The majority of the reported HIV infections were infected through injection drug use and most were young adults (unpublished data, China-MSD HIV/AIDS Partnership annual summary meeting, Liangshan Prefecture). Since the first HIV case reported in 1995, the Liangshan Prefecture has witnessed an alarming increase in HIV infection, and the HIV epidemic has spread to all 17 counties and cities.
The rate of HIV incidence has increased significantly in recent years, and it is calculated that the number of HIV infections in the past 5 years accounted for 81.5% of the total HIV/AIDS cases (unpublished data, meeting report of Liangshan Prefecture HIV epidemiological survey, Chinese National Center for AIDS/STD Control and Prevention). The spread of HIV infection is still extending in the Liangshan Prefecture, with some regions, such as Butuo and Zhaojue counties, affected seriously by HIV. The number of reported HIV/AIDS cases of Butuo, Zhaojue, Meigu, Yuexi, Jinyang, Ganluo counties and Xichang city accounted for 89.5% of the total cases (unpublished data, meeting report of Liangshan Prefecture HIV epidemiological survey, Chinese National Center for AIDS/STD Control and Prevention). The HIV epidemic of some of these counties has been studied and understood for a number of years, but little research has been undertaken on HIV in the Yanyuan and Muli counties, which are located at the western edge of the Liangshan Prefecture.
Liangshan is the largest autonomous prefecture of Yi nationality in China, with 46.5% of the population belonging to the Yi ethnic group. Among the Yi ethnic group, cultural traditions lead to more frequent casual sexual behavior among Yi males than Han males, and casual sex is also more frequent among unmarried Yi females than married Yi females. Thus, whether heterosexual transmission from persons infected through injection drug use is a major HIV transmission risk for the general population in the Liangshan Prefecture is important to identify.
Therefore, to gain a more accurate understanding of the HIV epidemic in the Yanyuan and Muli counties, the HIV risk factors and whether the HIV epidemic has spread from high-risk groups to the general population, the State Council the AIDS Working Committee Office, Ministry of Public Health and China CDC initiated and organized the Sichuan Province CDC, Liangshan Prefecture CDC, and Anhui Medical University to carry out an HIV epidemiological survey in the Yanyuan and Muli counties from July to October, 2009. Since HCV shares the same transmission routes with HIV [Verucchi et al., 2004], with HIV and HCV co-infection is common in injection drug users [Garten et al., 2005; Walsh et al., 2007]. Syphilis is an indicator of high-risk sexual behavior, and increase the risk of HIV transmission [Dyer et al., 1998]. Therefore, all the blood was tested for HIV, syphilis, and HCV in this study.
MATERIALS AND METHODS
Study Population and Data Collection Methods
To obtain a good representative sample of the overall population, a multistage stratified probability method was used to select participants in the Yanyuan county. First, all towns (N = 34) were stratified by the number of drug users and HIV reports in each town according to the nine strata shown in Table I. Second, one or more study town were selected at random from each of strata 1, 3, 5, 7, and 9. Third, one village were selected at random from the selected town, and a sample in each village of 300–500 subjects were recruited. If the population of the selected village was between 300–500, all residents of the village were investigated; if the population of the selected village was over 500, the village were stratified by village subgroup again to obtain a group of 300–500 people; if the population of the selected village was under 500, the nearest village was combined with the selected village to achieve a sufficient sample size. In the Muli county, the number of drug users was small and there were only 11 HIV reports by the end of June, 2009. Therefore, it is not necessary to stratify all towns by the number of drug users and HIV reports of each town according to the nine strata shown in Table I. In view of this, two towns (totally, there are 29 towns in the Muli county) were selected at random from Muli county first, then selected at random three villages from each of the selected towns again. In this study, people aged ≥ 2 years were included as the subjects, not only to understand the HIV epidemic in adults but also the HIV epidemic of mother-to-child transmission.
| Number of HIV reports | |||
|---|---|---|---|
| Many | Middle | Few | |
| Number of drug users | |||
| Many | 1 | 2 | 3 |
| Middle | 4 | 5 | 6 |
| Few | 7 | 8 | 9 |
A real-name registration and a confidential method were adopted during the study, in order to follow the persons infected with HIV conveniently in the future. Face-to-face interviews were implemented with a questionnaire after obtaining oral consent from the participants. The questionnaire included demographic information (such as name, age, gender, marital status, area of residence, and occupation) and risk behavior information (such as injecting drug use, needle sharing, multiple sex partners, and condom use). After the interview, a blood specimen was collected by a trained nurse and the specimen was labeled with a unique identification number, which was linked to the questionnaire by the unique identification number.
Laboratory Methods
All blood specimens were transported daily to the local CDC laboratory for HIV, syphilis, and HCV testing. Antibody to HIV was screened by ELISA (BioMérieux, Organon, Holland). If a sample screened HIV positive, two further assays (the original assay plus a different assay) were conducted in parallel. If both were negative, the result was considered as HIV negative. If both were positive or there was discordance in the results, a confirmatory test was done using a Western blot assay (Genelabs Diagnostics Pte Ltd, Cavendish, Singapore). Antibody to syphilis was screened by rapid plasma regain (RPR) card test (Zhuhai Lizhu Reagent Co., Zhuhai, China) and positive RPR tests were confirmed by Treponema pallidum particle assay (TPPA) test (Serodia TP-PA Fujirebio, Fuji, Japan). Antibody to HCV was screened by ELISA (Xiamen Yingke Xinchuang Technology Co., Ltd, Xiamen, China) and positive ELISA tests were confirmed by a second ELISA (Zhuhai Lizhu Reagent Co.). All screening tests were conducted at the Yanyuan CDC and the Muli CDC laboratories, respectively, and the screened positive samples were sent to the Liangshan Prefecture CDC for confirmatory test.
Data Analysis
Data were entered twice and evaluated for congruency using EpiData 3.1 software (The EpiData Association, Odense, Denmark) and analyzed using SPSS 10.01 software (SPSS, Chicago, IL).
Ethical Clearance
Ethical approval for the study was obtained from the Ethics Committee of China CDC, Liangshan Prefecture CDC, and local CDC before investigating. The study was done under the full knowledge and consent by participants, who were assured of the security of the information.
RESULTS
Demographic Characteristics
Ten villages were selected from the Yanyuan county and six villages from the Muli county. A total of 4,950 subjects participated in the study, including 3,404 participants from the Yanyuan county and 1,546 from the Muli county.
The mean age of the subjects was 30.89 years; 44.9% were males and 55.1% were females; and 73.2% were aged 15–49 years. Among the subjects aged ≥ 15 years (4,087), most were married (83.1%); nearly half of them (40.9%) were illiterates and 34.1% had only primary education; the most commonly reported occupation was farmer (90.7%), followed by student (6.7%). The ethnicity was dominated by Han and Yi ethnic group, accounting for 48.85% and 23.3%, respectively. Further description of demographic characteristics is presented in Table II.
| Characteristics | No. (%) |
|---|---|
| Gender | |
| Male | 2,223 (44.9) |
| Female | 2,727 (55.1) |
| Age (years) | |
| 2–14 | 863 (17.4) |
| 15–29 | 1,293 (26.1) |
| 30–44 | 1,943 (39.3) |
| 45–59 | 833 (16.8) |
| ≥60 | 18 (0.4) |
| Marital status (age ≥ 15 years) | |
| Married | 3,398 (83.1) |
| Unmarried | 625 (15.3) |
| Living together | 9 (0.2) |
| Divorce/widow | 46 (1.1) |
| Missing | 9 (0.2) |
| Education level (age ≥ 15 years) | |
| Illiterate | 1,671 (40.9) |
| Primary school | 1,395 (34.1) |
| Secondary school | 783 (19.2) |
| High school | 177 (4.3) |
| Higher | 60 (1.5) |
| Missing | 1 (0.0) |
| Ethnicity | |
| Han | 2,418 (48.8) |
| Yi | 1,154 (23.3) |
| Zang | 874 (17.7) |
| Miao | 49 (1.0) |
| Other | 453 (9.2) |
| Missing | 2 (0.0) |
| Occupation (age ≥ 15 years) | |
| Farmer | 3,705 (90.7) |
| Worker | 16 (0.4) |
| Cadre staff | 27 (0.7) |
| Medical staff | 36 (0.9) |
| Teacher | 13 (0.3) |
| Student | 274 (6.7) |
| Businessman | 9 (0.2) |
| Retired officer/unemployed | 6 (0.1) |
| Other | 1 (0.0) |
The proportions of all age groups are approximately balanced except the <5 and >60 age groups, which are presented in Table III.
| Age groups | Male | Female | Total |
|---|---|---|---|
| Number (%) | Number (%) | Number (%) | |
| ≤4 | 26 (1.2) | 21 (0.8) | 47 (0.9) |
| 5 | 166 (7.5) | 136 (5.0) | 302 (6.1) |
| 10 | 266 (12.0) | 248 (9.1) | 514 (10.4) |
| 15 | 221 (9.9) | 234 (8.6) | 455 (9.2) |
| 20 | 140 (6.3) | 187 (6.9) | 327 (6.6) |
| 25 | 217 (9.8) | 294 (10.8) | 511 (10.3) |
| 30 | 223 (10.0) | 323 (11.8) | 546 (11.0) |
| 35 | 314 (14.1) | 412 (15.1) | 726 (14.7) |
| 40 | 276 (12.4) | 395 (14.5) | 671 (13.6) |
| 45 | 158 (7.1) | 228 (8.4) | 386 (7.8) |
| 50 | 117 (5.3) | 146 (5.4) | 264 (5.3) |
| 55 | 86 (3.9) | 97 (3.6) | 183 (3.7) |
| ≥60 | 12 (0.5) | 6 (0.2) | 18 (0.4) |
Prevalence of HIV, Syphilis, and HCV
Of the 4,950 subjects tested for HIV, syphilis, and HCV, 2 (0.06%) were HIV positive, 2 (0.06%) were syphilis positive and 6 (0.12%) were HCV positive, and none of them were HIV/syphilis/HCV co-infection. These two HIV positive and two syphilis positive subjects were all from the Yanyuan county. Of the six HCV positive subjects, five came from the Yanyuan county and one came from the Muli county.
HIV prevalence in the Yanyuan county was 0.06% (95% CI: 0–0.142), syphilis prevalence was 0.06% (95% CI: 0–0.142), and HCV prevalence was 0.15% (95% CI: 0.020–0.280). HCV prevalence of Muli county was 0.06% (95% CI: 0–0.191), and none was found to be HIV or syphilis positive.
High-Risk Behaviors
Of the subjects aged ≥ 15 years (4,087), only 5 (0.12%) self-reported being drug users, 2 (0.05%) refused to response. Among these five drug users, two (40%) were injection drug users. But these two injection drug users both refused to respond whether they were sharing needles.
Of the subjects aged ≥ 15 years, only 19 (0.5%) self-reported having multiple sex partners, 13 (0.3%) refused to respond. Of the subjects who had multiple sex partners, only five (26.3%) used a condom during the last sexual intercourse, and two (10.5%) refused to respond. And, of these subjects (age ≥ 15), 149 (3.6%) self-reported working away from home last year, 12 (0.3%) refused to respond.
Behavioral Characteristics of Sero-Positive Subjects
Of the two HIV positive subjects, one was male and the other was female, both of them had been married and were Yi ethnicity, and their age were between 40 and 45 years. Neither of them self-reported being drug users nor having multiple sex partners.
Of the two syphilis positive subjects, one was male and unmarried, the other was female and married, both of them were Yi ethnicity and their ages were between 30 and 36 years. Neither of them self-reported being drug users; only the positive female self-reported multiple sex partners and not using a condom during the last sexual intercourse.
Of the six HCV positive subjects, five were male and one was female, four were married and two were unmarried. Four were of the Yi ethnicity, and the two others were of the Zang and Menggu ethnicity, respectively. Their ages were between 20 and 37 years. Five of them self-reported neither being drug users nor having multiple sex partners; only one self-reported being injection drug user, but not having multiple sex partners.
DISCUSSION
In this study, the proportions of all age groups were approximately balanced except the <5 and >60 age groups. A potential explanation was that all the chiefs of the selected villages were requested to assemble the villagers, then explain and promote the value of the study, in order to improve the participation of villagers and the balance of all age groups, and to reduce the selection bias. However, the <5 age group were too young to understand the objective and reasons of the study and they were afraid of blood drawing. Although consent could be obtained from their parents, most parents did not want their children to be bled. For people >60 age, most of them considered themselves to be old and were unwilling to blood drawing, which led to lower participation rates.
It was found that the HIV prevalence (0.06%) of Yanyuan county was close to the total population prevalence of China (0.05%) [State Council AIDS Working Committee Office UN Theme Group on AIDS in China, 2007]. Low levels of syphilis (0.06%) and HCV (0.15%) were also found, compared to the estimated syphilis average prevalence of Shenzhen (0.76%) [Hong et al., 2009] and the HCV overall average prevalence of China (0.58%) [Lu et al., 2009]. The cumulative number of persons infected with HIV reported in Yanyuan county was 137 by the end of June 2009, out of a total population 350,000 (0.04%), which is very consistent with this study. Through the end of June 2009, there were only 11 cumulative reported HIV infections in the Muli county, with a total population of 130,000 (0.01%). It is again consistent with this study finding and makes it not surprising that this study found no HIV infected persons. This study results further suggest that there are not a large number of undiagnosed or unreported HIV infections in these counties.
From the HIV case-reporting number in the Yanyuan county and the epidemiological survey results, it was known that the HIV epidemic of Yanyuan county is at an average level currently, compared to the overall HIV epidemic in the Liangshan Prefecture, and the rate in the Muli county is lower than average. These combined findings imply that the HIV epidemic has not spread from high-risk groups to the general population in either the Yanyuan county or the Muli county.
Of the participants aged ≥ 15 years, only 0.46% self-reported multiple sex partners and the condom use rate during the last sexual intercourse is low (26.3%), which implies that there are certain high-risk sexual behaviors among this population. And, although only 0.12% self-reported being drug users, the proportion of injection drug user is rather high (40%). For the sensitive nature of these questions, some may have underreported their risk behaviors during interviews, although some measures were taken to avoid this phenomenon. For example, nurses were requested to observe the participants' arms when collecting blood specimens to judge whether there was evidence of injection drug use. If injection drug use markings were found, they would make a mark on the questionnaire. However, for the multiple sex partners, condom use and needle sharing were reported by the participants. It is reported that among the case-reporting HIV infections in the Yanyuan and Muli county, 86.86% of them were infected via injection drug use and 5.84% were infected via sexual contact. These combined findings imply that the major route of HIV transmission is still through injection drug use, and sexual transmission has not become another major transmission route in these two counties.
None of the participants aged 2–14 years were found HIV positive in this study. And, it is reported that by the end of June 2009 only two pregnant women were found HIV positive for preliminary screening at antenatal clinic in the Yanyuan and none in the Muli county, which implies that the mother-to-child HIV infection rate is very low.
The HIV, syphilis, and HCV prevalence were not high in these two counties, and only little high-risk behavior had been reported. However, it is still necessary to strengthen the AIDS health education and prevention interventions for the high-risk groups in these two counties, to prevent the HIV spread from these groups to other groups.
Acknowledgements
We thank China CDC, Sichuan Province CDC, Liangshan Prefecture CDC, Yanyuan County CDC, Muli County CDC, and study participants for their keen cooperation.
