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High HIV Prevalence Detected in 2006 and 2007 Among Men Who Have Sex With Men in China's Largest Municipality: An Alarming Epidemic in Chongqing, China

Feng, Liangui MD, MS*; Ding, Xianbin MD, MPH*; Lu, Rongrong MD*; Liu, Jie MPH†; Sy, Aileen BA‡; Ouyang, Lin MD, MS*; Pan, Chuanbo MD, MPH§; Yi, Huirong MD‖; Liu, Honghong MD, MPH¶; Xu, Jing BS*; Zhao, Jinkou MD, PhD#

JAIDS Journal of Acquired Immune Deficiency Syndromes: September 2009 - Volume 52 - Issue 1 - pp 79-85
doi: 10.1097/QAI.0b013e3181a4f53e
Epidemiology and Social Science

Background: Data from many large cities in China show HIV prevalence among men who have sex with men (MSM) increasing dramatically over the recent years, making HIV transmission among MSM in China a growing concern. To facilitate targeted HIV prevention among MSM in Chongqing, surveys were conducted to examine HIV prevalence and its associated factors in 2006 and in 2007.

Methods: Surveys were conducted in 2006 and 2007 in 3 districts of Chongqing at venues and cruising areas where MSM frequent. Univariate and bivariate analysis were conducted on demographic, behavioral, and biological data.

Results: HIV prevalence was 19.7% in 2006 and 26.5% in 2007 among recruitees from bathhouses and saunas, more than 2 times higher than recruitees from other venues for both years. HIV prevalence increased from 10.4% in 2006 to 12.5% in 2007. HIV prevalence was more than 20% among those older than 40 years of age, much higher than HIV prevalence in younger age groups. HIV prevalence among married MSM was 15.9% in 2006 and 20.9% in 2007, compared with nonmarried MSM at 7.6% in 2006 and 9.2% in 2007.

Discussion: Urgent attention for prevention services is required to address the overall high HIV prevalence among MSM in the city, with special focus on subgroups as older, married MSM, and those recruited from bathhouses and saunas.

From the *Chongqing Municipal Center for Disease Control and Prevention, Chongqing, China; †Association of Schools of Public Health/CDC Allan Rosenfield Global Health Fellow, Atlanta, GA; ‡University of California, San Francisco, CA; §Yuzhong District Center for Disease Control and Prevention, Chongqing, China; ‖Jiulongpo District Center for Disease Control and Prevention, Chongqing, China; ¶Shapingba District Center for Disease Control and Prevention, Chongqing, China; and #Bill & Melinda Gates Foundation, Beijing, China.

Received for publication October 22, 2008; accepted March 6, 2009.

Supported by Global Fund for AIDS, Tuberculosis, and Malaria.

Correspondence address: Jinkou Zhao, MD, PhD, Bill & Melinda Gates Foundation, Beijing Representative Office, Suite 1201, China Resources Building, 8 Jianguomenbei Avenue, Beijing 100005, China (e-mail: jinkouzhao@hotmail.com).

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INTRODUCTION

Globally, unprotected sex between men is a major route of HIV transmission. In the United States, 49% of new HIV/AIDS diagnoses were among men who have sex with men (MSM) in 2006.1 In Asia, studies in Bangkok, Thailand, show that HIV prevalence among MSM increased from 17.3% in 2003 to 28.3% in 2005.2,3 MSM are becoming an increasingly critical population in China's HIV epidemic. In 2005, MSM transmission only accounted for 0.4% of the country's HIV cases, whereas in 2007, the proportion increased to 3.3%.4 Of the estimated 50,000 new HIV infections in 2007, 12.2% were thought to be MSM transmissions.4 After the country experienced the first wave of its HIV epidemic among injection drug users in southern China in the late 1980s and early 1990s and the second wave among former plasma donors in the 1990s, the MSM epidemic has the potential to be the next big wave.5

The MSM population in China is estimated by various studies to range from 5 million to 20 million.6-8 As growing public acceptance in China is allowing MSM to become better connected with each other and meet a great number of sex partners through the internet and increasing numbers of gay bars, clubs, and other venues, there is potential for rapid spread of HIV across the population. In contrast to countries in which the majority of MSM do not have sex with women, many MSM in China are married or have multiple female partners, increasing the possibility for greater heterosexual transmission.9,10

Although only 0.6% of the cumulative HIV cases in China are reportedly due to homosexual transmission, a growing number of studies in recent years support the upward trend of HIV prevalence among MSM in urban areas.4 In Beijing, MSM HIV prevalence increased from 0.4% in 2004 to 5.8% in 2006.11 In Chengdu, Sichuan, an increase was seen from 0.64% in 2003 to 9.1% in 2007 (Yuji Feng, Unpublished UCLA Dissertation “HIV/STD prevalence among MSM in Chengdu, China and associated risk factors for HIV infection”, 2008); in Shenzhen, Guangdong, from 1.75% in 2004 to 2.7% in 200612,13; and in Harbin, Heilongjiang, from 1.3% in 2002 to 2.2% in 2006.12,14 Geographic variability of HIV prevalence among MSM is apparent with some surveys finding few to no HIV cases.7,15,16

Syphilis reemerged as a public health problem in China in the 1980s after virtual eradication since the 1960s.17 Along with the overall reemergence of syphilis and increasing prevalence of HIV among MSM, a few recent studies in several Chinese cities reported high and possibly increasing prevalence of syphilis among MSM.18-21 These limited findings point to a possible synergic increase in HIV and syphilis epidemics in China now.

Chongqing is the largest municipality in China located in the southwest next to Sichuan province. With a total area of 82,400 Km2 covering 40 districts and counties, the municipality is home to 32 million residents, of which 3.9 million are migrants and 13 million reside in urban areas of the municipality.22,23 At the end of 2007, 3913 HIV cases were reported in the city, with MSM accounting for 8.6% of the reported HIV cases. By 2005, the MSM population size was estimated to be between 121,000 and 242,000, most of whom reside in urban districts [Dr. Xianbin Ding, MD, personal oral communication 2008, Chongqing Centers for Disease Control and Prevention (CDC)]. HIV and syphilis prevalence among MSM in Chongqing remains unknown. Only 1 small sample size (N = 256) survey conducted in 1 district in 2005 that found HIV prevalence to be 5.8% (Chuanbo Pan, unpublished data 2006).

To facilitate better targeting of HIV prevention, care, and treatment activities in the municipality, surveys were conducted to examine HIV prevalence and its associated factors, including syphilis, within the MSM population of Chongqing in 2006 and in 2007.

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METHODS

MSM were recruited between July and September of both 2006 and 2007. Subjects who were18 years or older, lived in Chongqing in the 3 months before the survey, and had oral or anal sex with a male in the last year were eligible.

An exercise was conducted in 2006 to map out all MSM activity venues, including clubs, bars, bathhouses, and outdoor cruising areas, known to peer educators. The same set of venues was used in 2007 for consistency.

Sample size was estimated based on the prevalence of HIV among MSM at 5.8% in 2005 (Chuanbo Pan, unpublished data 2006). MSM population size of 121,000 (personal communication with Dr. Xiaobin Ding, Chongqing CDC), alpha value of 0.05, and a power of 70%. Given these conditions, 690 subjects were required. Considering that nonprobability sampling was used and because HIV prevalence among MSM in 2005 was calculated from a very small sample, the sample size was increased to 1000 to allow for greater representativeness and possible high refusal rates.

Participants were recruited by venue-based and cruising area-based convenience sampling that was supplemented by community outreach, peer-recruitment, and web-based recruitment. Local CDC worked with trained MSM volunteers to recruit participants in venues and cruising areas known to be frequented by MSM in the 3 central districts of Chongqing where MSM venues concentrated. Venues and cruising areas were separated into bars, bathhouses and saunas, outdoor cruising areas such as parks and public bathrooms, and websites. In 2006, only 5 gay bars and 4 bathhouses were identifiable in the 3 districts covered, therefore, all sites were used for participant recruitment. Recruitment was conducted every Friday and Saturday night during the defined 2-month period during peak visiting/cruising hours. The same venues from 2006 were used in 2007 to keep data from these 2 years comparable. Web-based recruitment was conducted through advertisements placed on MSM websites.

MSM who were eligible and expressed willingness to participate via oral consent were administered a face-to-face questionnaire by trained interviewers. Questionnaires collected information regarding demographics, sexual behavior, drug history, general HIV knowledge, self-reported history of other sexually transmitted infections in the past 12 months, and history of receiving HIV prevention services during the past 12 months. HIV knowledge was assessed using 8 questions defined by the China HIV Monitoring and Evaluation Framework.24

After completion of the questionnaire, 3-5 mL of blood was collected from consenting individuals for HIV and syphilis testing. Enzyme-linked immunosorbent assay was performed in both 2006 (Shanghai Kehua Bio-engineering Co Ltd, Shanghai, China; Beijing BGI-GBI Biotech Co Ltd, Beijing, China; and Livzon Group Reagent Factory, Fuzhou, China) and 2007 (Shanghai Kehua Bio-engineering Co, Ltd, Shanghai, China) to screen for HIV antibody. Western blot test was performed using HIVBLOT 2.2 in 2006 and 2007 (Genelabs Diagnostics Pvt Ltd, Singapore) to confirm HIV antibodies. All HIV antibody test kits were recommended by the China National AIDS Reference Laboratory at Chinese CDC. Syphilis antibody was screened using Rapid Plasma Reagin in 2006 (Shanghai Kehua Bio-engineering Co, Ltd, Shanghai, China) and 2007 (Shanghai Kehua Bio-engineering Co Ltd, Shanghai, China). Confirmation was conducted using Treponema Pallidum Particle Agglutination assay in both years (Livzon Group Reagent Factory, Fuzhou, China).

Pretest and posttest counseling was conducted for all participants. Those who tested positive for HIV and or syphilis were referred to additional services. The protocol was approved by the Chongqing Municipal CDC.

EpiData 3.02 software (EpiData Association Odense, Denmark) was used for data entry. Statistical analysis was performed using SPSS 12.0 (SPSS Inc, Chicago, IL). Descriptive univariate analysis was conducted on demographic and behavioral characteristics. Demographic data from 2006 and 2007 were assessed for comparability between the 2 years. Although a nonprobability sampling method was used, the sample size was considered large enough to be representative of the population. Therefore, the data were analyzed using probability sampling statistical tests. Bivariate analyses were conducted separately for 2006 and 2007 data to analyze demographic and behavioral characteristics' correlations to HIV prevalence. All reported values are 2 sided, P values <0.05 were considered to be statistically significant.

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RESULTS

The total number of participating MSM was 1000 in 2006 and 1044 in 2007. The same protocol and survey instrument was used for both years. Across all categories, the demographics of the 2 years were very similar; the notable change was in the number of participants from each type of venue. An increased proportion of government employees was also found in 2007 (Table 1). Comparison of HIV-related behaviors between 2006 and 2007 also showed very little change overall, with differences only in the breakdown of number of male partners in the last 6 months and those who had an HIV test in the past (higher in 2007) (Table 1). A high percentage, 71.9%, of participants in both 2006 and 2007, had previously received HIV prevention services.

The increase in HIV prevalence was not statistically significant from 10.4% in 2006 to 12.5% in 2007 (P = 0.145). Syphilis infection rate did not decrease significantly from 9.3% in 2006 to 8.5% in 2007. The rate of HIV syphilis coinfection did not change significantly from 1.7% in 2006 to 2.7% in 2007 (P = 0.130) (Table 2). Analysis of HIV prevalence in each of the demographic and behavioral categories demonstrated several consistencies between 2006 and 2007 (Table 3). Higher HIV prevalence was found among those recruited from bathhouses and saunas than other venues or outdoor cruising areas. HIV prevalence increased with older age groups (P < 0.001 for both 2006 and 2007). Those with less education were more likely to be infected (P < 0.001 for both 2006 and 2007). In both years, there was no significant difference in HIV prevalence between migrant and nonmigrant populations. HIV prevalence was significantly higher in subjects recruited from bathhouses and saunas. Married MSM were more likely to be affected than singles, with 22.4%-7.5% in 2006 and 21.8%-9.3% in 2007. Compared with unmarried MSM, married MSM had poorer knowledge of HIV (85.9% vs. 91.3% in 2006; 79.1% vs. 93.5% in 2007; P < 0.01 for both years), higher unprotected anal sex in the past 6 months (76.8% vs. 65.4% in 2006; 79.6% vs. 58.0% in 2007; P < 0.01 for both years), and poorer access to intervention services (64.3% vs. 74.4% in 2006; 59.2% vs. 76.9% in 2007; P < 0.01 for both years) in both 2006 and 2007.

Changes in HIV prevalence between 2006 and 2007 was most marked in the increased HIV prevalence among those who had sex with a female in the last 6 months, from 12.4% in 2006 to 21.6% in 2007 (Table 3), with most of the positive subjects engaged in unprotected sex with females (24 of 30 cases, 80% in 2006 and 48 of 56 cases, 86% in 2007). The increase from 2006 to 2007 was observed for both, those with 1 and greater than 1 female sex partner in the last 6 months, but the increase was greatest among MSM who had only 1 female sex partner in the last 6 months. Further analysis revealed that of these HIV cases, the single female sex partner was most commonly a spouse (35 of 47 or 74% of HIV cases in 2007). From 2006 to 2007, there was also a reversal in the trends of HIV prevalence in relationship to age of first sexual contact with a higher HIV prevalence in subjects who first engaged in sexual activity at a younger age in 2007. Although HIV prevalence was similar in 2006 and 2007 in men who self identify as homosexual, HIV prevalence in those who self identified as heterosexual or bisexual greatly increased from 10.4% in 2006 to 18.6% in 2007. Additionally, much of the overall increase in HIV prevalence from 2006 to 2007 was found to be in those younger than the age of 25 years (P = 0.03).

In line with HIV prevalence stratified by demographic and behavioral factors, a similar pattern was found for prevalence of syphilis when analyzed by the demographic and behavioral categories. Higher syphilis prevalence was found among those who were recruited from bathhouses, older age groups, less educated, and HIV positive (data not shown).

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DISCUSSION

In both 2006 and 2007, our survey found consistently high overall HIV prevalence among MSM in Chongqing. Both figures are the highest reported in China for HIV prevalence in MSM surveys conducted in these 2 years.

Analysis by demographic and behavioral characteristics indicated disproportionately high HIV prevalence in certain subgroups. MSM recruited from bathhouses and saunas were more likely to be HIV positive than MSM recruited from other venues. As previous studies have found recent sex at a bathhouse to be a significant source of HIV exposure in the MSM population, our finding of an elevated HIV prevalence in this subgroup demonstrates the potential of venue-focused interventions for curbing HIV transmission in the Chongqing population.25

Our study also found a higher HIV prevalence in married over single MSM, with prevalence more than twice as high in those who are married than single in both years. Many studies characterizing the MSM population in China have found that the majority of older MSM are married and have cited this as a concern for HIV transmission to low-risk female spouses and children.10 So far, few studies have been able to analyze HIV prevalence in married versus single MSM. In Beijing, HIV prevalence was shown to be higher in single than in married MSM in both 2005 (3.7% single to 0.9% married) and 2006 (6.8% single to 4.9% married).11 Our finding of significantly higher prevalence in married MSM, despite having at least 3 times more single than married MSM participating in each year's study, substantiates the real possibility of married MSM as a bridge for HIV transmission to the heterosexual population. HIV prevalence was higher in 2007 among those who self identify as bisexual. As a result of strong cultural and family pressures, many Chinese MSM are compelled to be married and to have a child to carry on the family name. They frequent MSM venues less and typically do not have a regular partner. Our results also show that married MSM have poor knowledge of HIV, lower rate of condom use, and poorer access to intervention services than young and unmarried MSM in the city in both 2006 and 2007. This further underscores the urgent need to address HIV in the MSM population to prevent an ensuing heterosexual epidemic.

Several other subgroups with significantly higher HIV prevalence corresponded to HIV vulnerable subpopulations previously found in MSM surveys conducted in other areas of China. Those of lower education, those who were unemployed or of atypical employment, those with larger number of male partners, and those of older age were all found in both 2006 and 2007 to have higher HIV prevalence. Interestingly, a significant change in HIV prevalence between 2006 and 2007 was seen in the category of age, where HIV prevalence in the younger than 18 age group increased from 9.1% in 2006 to 14.5% in 2007. This rising HIV prevalence in younger MSM has been seen in other regional MSM surveys and may suggest a growing number of new infections.11

Several subgroups of the study did not follow expected HIV prevalence trends. HIV prevalence was not higher in MSM without Chongqing residency compared with those with Chongqing residency (hukou). Higher HIV prevalence has commonly been expected in migrant MSM: a study in Jinan found that men without residency were more likely to engage in unprotected anal intercourse; another study in Beijing found a larger increase in HIV prevalence in those without Beijing residence status than in those with.11,26

The proportion of those who have tested for HIV previously increased substantially from 2006 to 2007 (from 18.9% to 35.2%). The scale-up of HIV testing after high prevalence discovered in 2006 may account for this increase. Syphilis coinfection showed strong correlation with HIV infection in both 2006 (P = 0.009) and 2007 (P = 0.039) (Table 3). HIV and syphilis infections are found to be mutually independently associated with each other. Syphilis infection facilitates acquisition and transmission of HIV, and HIV can alter the natural course of syphilis. Early treatment of syphilis is crucial as it reduces the risk of HIV transmission.

Due to the discreet nature of the MSM population in Chongqing and our limited knowledge about them at the time the study commenced, we pursued a venue-based approach supplemented by recruitment through peers and on the web. Although a probability sampling method was not used, we increased the sample size from the calculated 690 to 1000 so that the sample size is large enough to be representative of the population. In the future, other sampling methods will be explored as an alternative to the method used in this study to assess its utility among MSM. When we compare the sample composition of the 2 years, the proportion of recruited subjects from the 3 venue categories differed significantly from 2006 to 2007. About 17% more subjects were recruited from outdoor cruising areas and the web in 2007. However, similar patterns of HIV prevalence appeared across the venue categories, with bathhouses and saunas having the highest, gay bars in the middle, and outdoor cruising area and websites the lowest. Other major characteristics of the samples were similar enough that we considered the 2 years comparable. The study questionnaire did not differentiate insertive and receptive unprotected anal sex. Thus we were not able to examine the correlations on disease outcomes related to sexual role.

One of the strengths of the study lies in the consistency of methods used in both years. The sampling method and the questionnaire were exactly the same over the 2 years. The same group of interviewers and the same laboratory procedures were used, ensuring consistent quality in the data collected. Over the course of the study, the Chongqing CDC's success in establishing rapport with the MSM community has led to greater mutual understanding and greater community participation in the city's HIV prevention efforts. This progress will enhance the Chongqing CDC's ability to develop more effective interventions for the MSM population.

Our study has found that HIV prevalence is alarmingly high in the MSM population in Chongqing. Particular subgroups are at especially high risk, including those who frequent bathhouse/saunas, those who do not self-identify as homosexual, older, married MSM and those who are syphilis positive. These findings point to a great need for behavioral interventions to focus on the potential bridging sub-groups to prevent the fueling of a heterosexual epidemic. These results can be incorporated into Chongqing CDC's HIV program planning and targeting, so as to match resources with needs. Nationally, scale-up of prevention and HIV testing among MSM in major urban areas, along with appropriate treatment and care services, must be prioritized in order to effectively control the spread of the epidemic in the MSM population.

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ACKNOWLEDGMENTS

We would like to thank the Global Fund for AIDS, Tuberculosis, and Malaria for funding this study. We also thank local CDC staff at 3 district CDCs in Chongqing for their participation in the field data collection. Special thanks to Dr. Marc Bulterys for his valuable comments. We feel indebted to MSM volunteers and venue owners who help the mobilization and organization efforts during the field surveys and subjects who voluntarily participated.

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Keywords:

China; Chongqing; epidemiology; HIV-1; MSM; syphilis

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