WU, ZUNYOU PhD*; ROTHERAM-BORUS, MARY JANE PhD†; LI, LI PhD†; GUAN, JIHUI MD‡; DETELS, ROGER PhD§; YIN, YUEPING PhD|; WU, SHENG MPP†; LIU, ZHENDONG MD*; LIN, CHUNQING MD§; HSIEH, JULIE MPH§; THE NIMH COLLABORATIVE HIV/STD PREVENTION TRIAL GROUP
From the *National Center for AIDS/STD Control and Prevention, Chinese Centers for Disease Control and Prevention, Beijing, China; †Center for Community Help, Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, Los Angeles, California; ‡Fujian Center for Disease Control and Prevention, Fuzhou, China; §School of Public Health, University of California, Los Angeles, Los Angeles, California; and |National STD Reference Laboratory, Nanjing, China
This study was funded by National Institute of Mental Health grant number U10MH61513, a 5-country Cooperative Agreement being conducted in China, INia, Peru, Russia, and Zimbabwe.
Each site has selected a different venue and population in which to implement the Community Public Opinion Leader (C-POL) intervention. The authors thank the team members in Fuzhou, Nanjing, and Beijing, China, for their support and contributions to the study.
Correspondence: Li Li, PhD, Center for Community Health, University of California, Los Angeles, 10920 Wilshire Blvd., Ste. 350, Los Angeles, CA 90024. E-mail: firstname.lastname@example.org.
Received for publication April 11, 2007, and accepted June 14, 2007.
OVER THE PAST 20 YEARS, sexually transmitted diseases (STDs) have been given increasingly more attention in China. Studies conducted with different populations have yielded various results, but the overall trend is that STD rates have been rising.1–7 This increase is connected to changing attitudes toward and practices of sexual behavior, especially among China’s younger generation.8
A number of individual characteristics, such as gender and occupation, and behavioral factors, such as multiple sex partners and engaging in commercial sex, are believed to contribute to STD infection risk in China. From 1989 to 1998, STDs in China increased more in women than in men.1 Female sex workers, men who have sex with men, rural-to-urban migrant workers (e.g., construction workers, factory workers), and male migrants who patronize commercial sex workers have higher STD rates and are associated with greater risk behaviors.3–5,9–12 Extramarital relationships are a more common source of STD infection among the general public from 1995 to 1998.1 Parish and colleagues discovered that unprotected sex with a sex worker and less education were found to be risk factors for chlamydia infection in men, whereas less education, living in a city or along the southern coast, and having a spouse who earned high income were risk factors for chlamydia infection in women.2
Much of the variances in the prevalence of STD across studies can be accounted for by differences in study populations and sampling. For example, some studies were conducted with high-risk groups, such as patients at STD clinics or commercial sex workers. In contrast, the population reported in this study consists of market vendors and is relatively representative of the general population in urban centers of China. We report the prevalence and patterns of STDs and the relationships between STD status and demographic and behavioral factors among 4510 market vendors in eastern China.
Materials and Methods
Study Background and Population Selection
This study is part of a National Institute of Mental Health Collaborative HIV/STD Prevention Trial taking place in 5 populations at risk of HIV and STDs in China, India, Peru, Russia, and Zimbabwe. The trial used the Community Popular Opinion Leader model community-level HIV prevention intervention, which has shown success in risk reduction among populations vulnerable to HIV risk behavior in the United States and has the potential to be applied in a variety of international settings.13 The study phases consist of an ethnographic study, pilot studies, and a randomized controlled trial. This article will focus on results from the baseline assessment documenting risk among market vendors.
This study was conducted in markets in Fuzhou City, the capital of Fujian Province, eastern China. Normally a market has 50 to 150 stalls, with a total of 150 to 300 stall owners and employees. Social activities for market vendors usually center within a few blocks of each market, as they usually live close to work and socialize within that area. Participants for this study were recruited from 40 local food markets. The market selection was based on the size and geographic location of the markets. All vendors aged 18 to 49 years in the selected market were invited to participate in the study.
Gatekeepers, primarily government officials, and market managers were enthusiastic about gaining access to the study. The purpose of the study and the type of recruitment activities were announced in the market the day before data collection began. After informed consent was obtained, participants were transported by van to the Institute of Health Education of the City Center for Disease Control and Prevention (CDC) for behavioral risk assessment and collection of biologic specimens. All participants were paid 20 yuan (US $2.50) in cash for their participation. The study only used materials and procedures that had been approved by institutional review board at both the University of California, Los Angeles, and China CDC.
Collecting Behavioral Data
The survey questionnaire was administered in a private office face-to-face with interviewers recording responses on laptop computers. A preliminary study comparing the appropriateness of using computer-assisted personal interview (CAPI) versus audio computer-assisted self-interview showed that CAPI was much more suited for the market vendor population.14 The CAPI was developed to automatically incorporate skip patterns and logistic check to reduce human errors. With regard to sensitive sexual activities, interviewers clarified answers such as number of sexual partners and condom use, and the confirmed number reported was used in the analysis. Participants were also asked about the number of sexual partners in the past 6 months. For those persons having multiple partners (i.e., more than one), we further queried how many times the participant had sex with each nonprimary partner and how many time condoms were used within the past 6 months. If the number of times of having sex was greater than the number of times of using condoms within the past 6 months with nonprimary sexual partners, the participant was coded as having unprotected sex within the past 6 months. Alcohol use was defined as drinking alcohol at least once a month. Five demographic variables were also employed: age, gender, marital status, education, and self-reported discretionary income per month.
Collecting Biologic Data
Venous blood samples were collected to test for syphilis, herpes simplex virus type 2 (HSV-2), and HIV. Urine specimens were also collected from men and vaginal swabs were collected from women for chlamydia and gonorrhea testing. Trichomonas testing was performed on women only. All initial tests were performed at the Fujian Hospital for Sexually Transmitted Diseases and the STD laboratory at the National Center for STD and Leprosy Control in Nanjing. Quality control retests were performed by the Study Reference Lab at The Johns Hopkins University. Participants with nonviral positive STD results received treatment and counseling. HIV-positive participants received counseling and were referred to the local CDC for CD4 assessment and free antiretroviral treatment, and HSV-2-positive participants received treatment referral and counseling. All treatment procedures followed the study protocol and China CDC guidelines.
The main biologic measure of this study was STD status, which was defined as a positive result for chlamydia, gonorrhea, syphilis, trichomonas, HSV-2, or HIV following standardized laboratory protocols. Chlamydia and gonorrhea were tested using polymerase chain reaction. The MRL Diagnostics HSV-2 IgG test was used to identify specimens with positive HSV-2 antibody. HIV testing was performed using EIA or ELISA and repeated using a separate EIA/ELISA; positives were confirmed by Western blot analysis. Syphilis testing was performed by rapid plasma reagin and confirmed using the Treponema pallidum particle agglutination test. Vaginal swabs were cultured for Trichomonas vaginalis using the InPouch TV test.
All analyses were performed using SAS statistical software version 9.1.3 (SAS Inc., Cary, NC). First, descriptive analyses were performed to determine the prevalence of STDs based on laboratory results, and frequency distributions of STDs were tabulated by selected background factors. Second, risky behaviors and specific STDs were compared for men and women using χ2 tests. Third, Pearson correlation coefficients were calculated to investigate relationships between any STDs and participants’ demographics and risky behaviors. Finally, multiple logistic regression was performed to examine independent associations between STDs and participant age, gender, education, marital status, alcohol use, multiple sexual partners, and having any unprotected sex during the past 6 months. The respective odds ratios (ORs) and 95% confidence intervals are also reported.
Table 1 summarizes the sample’s characteristics. More than half of the participants were women; 82.4% were currently married or living with a partner, and 12.9% had an education level of high school or above. Frequency distribution of having STDs and its relationship with demographics and risky behaviors of study participants are presented (Table 1). The overall STD prevalence among market vendors was 16.5%. Three factors were associated with high rates of STDs: (1) older age; (2) being widowed, separated, or divorced; and (3) having higher discretionary monthly income. The STD rate was higher in women than men for chlamydia (11.2% vs. 6.3%), gonorrhea (1.36% vs. 0.6%), and HSV-2 (8.2% vs. 4.7%); χ2 tests revealed that the prevalence of any STDs was significantly higher for women than that for men (21.0% vs. 11.5%). Both the illiterate and those with an education of college and above were found to have a higher prevalence of STDs. Analyses remained unchanged when trichomonas was excluded from the list of STDs for women.
Risk behavior variables and specific STD infection by gender are also presented (Table 2). About 5.4% of the sample reported having more than 1 sexual partner during the past 6 months, and 7.5% reported having unprotected sex with someone other than a spouse or live-in partner during the past 6 months. Among participants who reported having more than 1 sexual partner during the past 6 months, 27.4% tested positive in at least 1 of the STD tests, and among those who reported having unprotected sex, 24.3% were found to have at least 1 STD. In this study, sexual risk behavior was significantly higher for male participants than female participants. Among those who reported having more than 1 sexual partner during the past 6 months, 91.3% were male, and among those who reported having unprotected extramarital sex, 81.9% were male.
Correlation coefficients of identified variables are reported (Table 3). Women were less likely than men to report multiple sexual partners, unprotected sex, and alcohol use. Having more discretionary money per month was positively correlated with alcohol use, multiple sexual partners, and unprotected sex during the past 6 months. Participants who consumed alcohol at least once in the previous month reported more sexual risk than those who did not. STD infection was significantly associated with multiple sexual partners and unprotected sex during the past 6 months.
Table 4 summarizes the results of multiple logistic regression analyses. When all were held constant, female gender and more than 1 sexual partner within past 6 months continued to be the 2 most important factors in predicting STDs (OR = 2.35 and 2.01, respectively). Unprotected sex during the past 6 months (OR = 1.62) was also significant. Having discretionary money and years of completed school remained significantly associated with STD status.
A previous study has reported a high prevalence of STDs among commercial sex workers in China (syphilis, 14%; chlamydia, 32%; gonorrhea, 8%; trichomonas, 12.5%).9 In this study, we found that women had a higher STD rate than men. This is consistent with previous findings of STD prevalence in Chinese women.1,4 STDs in women are often asymptomatic, perhaps making them less likely than men to notice the infection and to seek medical care. Women reported lower sexual risk (e.g., multiple sexual partners, unprotected sex with nonspouse, alcohol use), and more women were married in our sample, and therefore, it is probable that the higher STD rates among women were acquired through their husbands or regular sexual partners who engaged in high-risk behavior. Alternatively, women reported less extramarital partners, and may have been less likely to report their risky sexual behaviors. Moreover, because women play a passive gender role in traditional Chinese culture, they often have less access to information and skills to negotiate condom use with their sexual partners. This is further compromised by women’s economic dependency on their male counterparts and the fact that they have little power to negotiate safe sex practices. This makes addressing gender equality and educating women on sexual health a priority in public health interventions.
Having more than 1 sexual partner in the past 6 months, having unprotected sex with a nonspouse in the past 6 months, and drinking alcohol continued to be significant factors in predicting STD prevalence. These risky sexual behaviors have long been proven to be associated with higher STD prevalence. STD prevention and education programs need to focus on educating the general public in these areas as well as to raise their awareness of potential risks and the need for condoms.
With the opening of markets and society in the early 1990s, China has gone through a major transformation economically that has markedly influenced the social environments throughout major metropolitan areas as well as in small townships in rural areas, changes that have been observed on the individual level throughout the country.15 Young people are initiating sex at an earlier age, individuals are having more sex partners, and access to commercial sex is on the rise. These factors have important policy implications for the government in regulating entertainment industries to reduce risky sexual behaviors as well as to design appropriate sex education to promote delayed sexual debut among young adults and adolescents. In addition, special considerations are needed for low- versus high-education groups as well as men versus women to maximize the effects of prevention programs and messages.
Market vendors with more discretionary income were at higher sexual risk, a trend that has been observed in previous studies.2 This is consistent with the explanation that extra money allows individuals to engage in risky behaviors such as drinking alcohol and visiting entertainment industry venues. Multivariate analyses found that education was associated with both risk behaviors and STDs. Moreover, study participants who had no schooling and participants who had college or higher level of schooling reported a similarly high STD prevalence (26.19% vs. 24.00%, respectively). Participants with no schooling may have limited access to health care, and also may have difficulty understanding health or STD prevention messages, lack knowledge to engage in safe sex practices, and are less likely to recognize STD symptoms and seek treatment. STD prevention and education programs need to take these factors into consideration to target messages for groups with different education backgrounds.
Discussion of sexual behavior is a sensitive topic in China; thus, accurate information related to this subject is hard to obtain. As a result, the proportion of study participants engaging in high-risk sexual activities is likely to be higher than reported, although preventive measures such as extensive interviewer trainings and CAPI questionnaires were put in place. In addition, the data were collected in 1 geographic region of China and with only market vendors, and thus, the findings may not be generalizable to other areas and for people with other occupations.
In summary, our study identifies important policy implications as well as specific strategies for STD prevention and control for the Chinese government. Our findings that women are more vulnerable to acquire sexually transmitted infections suggest that more educational programs should target this group. In addition, when designing STD prevention messages, different education levels need to be considered in order to maximize impact. The entertainment industries may need more stringent regulation in order to reduce risky sexual behavior and halt the rapid spread of STDs.
1. Chen XS, Gong XD, Liang GJ, et al. Epidemiologic trends of sexually transmitted diseases in China. Sex Transm Dis 2000; 27:138–142.
2. Parish WL, Laumann EO, Cohen MS, et al. Population-based study of chlamydial infection in China: A hidden epidemic. JAMA 2003; 289:1265–1273.
3. He N, Detels R, Zhu J, et al. Characteristics and sexually transmitted diseases of male rural migrants in a metropolitan area of Eastern China. Sex Transm Dis 2005; 32:286–292.
4. Detels R, Wu Z, Rotheram MJ, et al. Sexually transmitted disease prevalence and characteristics of market vendors in eastern China. Sex Transm Dis 2003; 30:803–808.
5. Hesketh T, Li L, Ye X, et al. HIV and syphilis in migrant workers in eastern China. Sex Transm Infect 2006; 82:11–14.
6. Zhang KL, Ma SJ, Xia DY. Epidemiology of HIV and sexually transmitted infections in China. Sex Health 2004; 1:39–46.
7. Chen ZQ, Zhang GC, Gong XD, et al. Syphilis in China: Results of a national surveillance programme. Lancet 2007; 369:132–138.
8. Ma Q, Ono-Kihara M, Cong L, et al. Sexual behavior and awareness of Chinese university students in transition with implied risk of sexually transmitted diseases and HIV infection: A cross-sectional study. BMC Public Health 2006; 6:232.
9. Van den Hoek A, Fu Y, Nicole HT, et al. High prevalence of syphilis and other sexually transmitted diseases among sex workers in China: Potential for fast spread of HIV. AIDS 2001; 15:753–759.
10. Jiang J, Cao N, Zhang J, et al. High prevalence of sexually transmitted diseases among men who have sex with men in Jiangsu Province, China. Sex Transm Dis 2006; 33:118–123.
11. Wang B, Li X, Stanton B, et al. HIV-related risk behaviors and history of sexually transmitted diseases among male migrants who patronize commercial sex in China. Sex Transm Dis 2007; 34:1–8.
12. Liu H, Li X, Stanton B, et al. Risk factors for sexually transmitted disease among rural-to-urban migrants in China: Implications for HIV/sexually transmitted disease prevention. AIDS Patient Care STDS 2005; 19:49–57.
13. Kelly JA, Murphy DA, Sikkema KJ, et al; Community HIV Prevention Research Collaborative. Randomised, controlled, community-level HIV-prevention intervention for sexual-risk behaviour among homosexual men in US cities. Lancet 1997; 350:1500–1505.
14. Li L, Wu Z, Rotheram-Borus MJ, et al. Measuring sexual risk using audio-computer assisted self-interviewing (ACASI) vs. computer-assisted personal interview (CAPI) in China. J Psychol Human Sex 2007; 19:25–30.
15. Fuligni AJ, Zhang W. Attitudes toward family obligation among adolescents in contemporary urban and rural China. Child Dev 2004; 75:180–192.