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Incidence of HIV-1, Syphilis, Hepatitis B, and Hepatitis C Virus Infections and Predictors Associated With Retention in a 12-Month Follow-Up Study Among Men Who Have Sex With Men in Beijing, China

Ruan, Yuhua MD, PhD*; Jia, Yujiang MD, DrPH†‡; Zhang, Xiaoxi MD, MPH§; Liang, Hongyuan MD*; Li, Qingchun MD, MPH*; Yang, Ye MD; Li, Dongliang MD, MPH; Zhou, Zhenhai MD*; Luo, Fengji MD, MPH; Shi, Wei MD; Shao, Yiming MD, PhD*

JAIDS Journal of Acquired Immune Deficiency Syndromes: December 2009 - Volume 52 - Issue 5 - p 604-610
doi: 10.1097/QAI.0b013e3181b31f5c
Epidemiology and Social Science

Objective: To investigate the incidence of HIV-1, syphilis, hepatitis B virus (HBV), and hepatitis C virus (HCV) infections and predictors associated with retention in a 12-month follow-up study among men who have sex with men (MSM) in Beijing, China.

Methods: A total of 507 eligible seronegative MSM were enrolled. Study participants were tested for HIV-1, syphilis, HBV, and HCV and counseled at the baseline, 6-month, and 12-month follow-up visits. The retention rates were analyzed as a function of demographic, behavioral, and recruitment variables.

Results: Of the 507 participants, 86.2% (437) were retained in the cohort at the 12-month follow-up visit. The incidence rates were 2.6 per 100 person-years [95% confidence interval (CI): 1.1% to 4.1%] for HIV-1 infection, 16.9 per 100 person-years for syphilis (95% CI: 12.4% to 21.3%), 3.3 per 100 person-years for HBV (95% CI: 1.5% to 5.1%), and 0.2 per 100 person-years for HCV (95% CI: 0% to 0.7%). Higher education (adjusted odds ratio = 1.94, 95% CI: 1.03 to 3.66) and appearing at the 6-month follow-up visit (adjusted odds ratio = 26.15, 95% CI: 13.44 to 50.89) were significantly associated with 12-month retention.

Conclusions: HIV, syphilis, and HBV incidence are high among MSM. Intensified intervention is needed urgently. Widespread screening for HIV, syphilis, HBV, and HCV in this group should be considered as measures for control.

From the *State Key Laboratory for Infectious Disease Prevention and Control, and National Center for AIDS/sexually transmitted disease Control and Prevention, Chinese Center for Disease Control and Prevention (China CDC), Beijing, P. R. China; †Institute for Global Health; ‡Department of Pediatrics, Vanderbilt University School of Medicine, Nashville, TN; and §Chaoyang Center for Disease Control and Prevention, Beijing, People's Republic of China.

Received for publication January 14, 2009; accepted May 29, 2009.

This study was supported by grants from the Ministry of Science and Technology of China (2007DFC30230), by the National Institutes of Health (grants #R01 AI078933 and #R03AI073134), and the Institute for Global Health and Department of Pediatrics, Vanderbilt University School of Medicine, Nashville, TN.

Correspondence to: Yiming Shao, MD, PhD, State Key Laboratory for Infectious Disease Control and Prevention and National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, 27 Nanwei Road, Xuanwu District, Beijing 100050, People's Republic of China (e-mail:

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Injection drug use (IDU) and unhygienic plasma collection have been the 2 major transmission routes of HIV/AIDS in China since the country's first large outbreak was identified in 1989 among IDUs in southwestern Yunnan Province.1-3 In recent years, however, the risk of sexual transmission of HIV has grown, either through heterosexual contacts or unprotected homosexual sex between men.3 Among the estimated 700,000 people in China living with HIV/AIDS in 2007, 40.6% were infected through heterosexual transmission and 11.0% through homosexual transmission.3 Men who have sex with men (MSM) have newly emerged as a high-risk group in China. Homosexual transmission has primarily been documented in large and middle sized cities with large concentrations of migrants.4-10 National estimates and local projections suggested that 2%-5% of males are MSM, varying by urban and rural areas and by economic conditions.6 In 2007, the estimated HIV cases who were MSM were about 30,000 more than the 2005 estimate. The proportion of reported HIV cases among MSM increased 8-fold from 0.4% in 2005 to 3.3% in 2007.1 Because of the large size of the population, a small increase of HIV prevalence in MSM in China would mean a large increase in the number of domestic infections and a significant contribution to the total number of infections around the world.

Since adopting a free market economy and an open door policy in 1978, China has observed a remarkable increase in sexually transmitted diseases (STDs) besides HIV because of the change in social norms and sexual behaviors and because of population shifts due to migration.11 The first resurgent cases of syphilis were recognized in China in 1979, and the national surveillance data in China has demonstrated a steady and disturbing spread of this disease throughout the country. The annual reported incidence (per 100,000) of syphilis increased from 0.02 in 1985 to 0.23 in 1990 and rapidly rose to 6.43 in 2000 and 13.35 in 2006.12 Ulcerative STDs like syphilis are of particular concern, as they have been found to increase the likelihood of HIV seroconversion by 2-5 times.13-15 HIV infection, in turn, may increase the acquisition of other STDs and alter the natural history and response to the standard therapy of ulcerative STDs, resulting in “epidemiological synergy” between HIV and other STDs.16,17

In many countries, MSM behaviors are highly stigmatized, and MSM face strong social pressure. Such social environments may lead MSM to hide their sexual orientation and thus remain hard to reach by intervention programs.18,19 The traditional Chinese culture does not openly endorse MSM behaviors; MSM are still socially marginalized and a stigmatized group in the society.18,20 Data on HIV and syphilis prevalence and risk factors for both infections among MSM are increasingly available from cross-sectional studies and demonstrate a potential rising prevalence of HIV infection and consistently high prevalence of syphilis infection among MSM in China.9,14,21-25 However, little is known about the incidence of HIV-1, syphilis, hepatitis B virus (HBV), and hepatitis C virus (HCV) among MSM in China. So far, no study has been conducted to evaluate the predictors of retention in an MSM prospective cohort; such information would be helpful in developing the best possible prevention programs to slow down the epidemic's spread. The present study aimed to assess the incidence of HIV-1, syphilis, HBV, and HCV and examine the predictors associated with retention in a 12-month follow-up study among MSM in Beijing, China.

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Study Design and Study Participants

This prospective cohort study was conducted among MSM in Beijing, the capital of China. A baseline screening survey was conducted from November 2006 to February 2007. Study participants were recruited using 3 methods. First, study participants were recruited through a website advertisement by a nongovernmental AIDS volunteer group ( Second, peer recruiters were hired and trained to distribute flyers with study-related information at MSM-frequented venues, for example, MSM clubs, bars, parks, and bathhouses. Third, study participants were encouraged to refer their peers to attend the study. All potential participants came to a district HIV testing and counseling clinic in downtown Beijing for eligibility assessment. Eligibility criteria required that participants be HIV-seronegative, 18 years or older, male, have had anal or oral sex with another male in the past 3 months, and be willing to finish the 12-month follow-up study and provide written informed consent. A total of 541 MSM were screened: 4 did not meet eligibility criteria, 4 refused to participate in the 12-month follow-up study (0.7% refusal rate), and 26 (4.8% prevalence rate) were HIV positive and therefore were excluded. A total of 507 eligible and consenting MSM were enrolled into the prospective cohort. Participants were asked to come back to the designated clinic for follow-up evaluation every 6 months. Written informed consent was obtained from all eligible participants before being interviewed. Those who met the screening criteria then completed an HIV/STD risk assessment interview. At the end of the interview, client-centered risk reduction counseling was provided on HIV, HBV, HCV, syphilis infections, and other STDs. Blood samples were tested for HIV, syphilis, HBV, and HCV infections. Posttest counseling was also offered when they returned for their HIV test results. The study was approved by the institutional review boards of the National Center for AIDS/STD Control and Prevention of the China Center for Disease Control and Prevention.

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Cohort Retention Plan

A written procedure was followed in maintaining high retention rates at follow-up visits. All participants were asked to provide at least 2 different contact sources. This locator information was managed by the participant information file system (PIFS) software program. Whenever possible, the follow-up visits were to be scheduled on the “scheduled date.” Appointment reminder procedures at every 6-month follow-up visit included the following:

  1. Study staff sent cell phone, email, and/or internet messages via QQ (Tencent Inc, Beijing, China) or MSN (Web Messenger; Microsoft Corporation, Seattle, WA) to the participant 2-3 weeks before the scheduled visit. Study staff also contacted the participant on the week of the scheduled study visit to confirm that the participant planned to keep the appointment.
  2. Study staff would call the participant on the same day and reschedule an appointment for the next working day when a participant missed an appointment.
  3. If the participant was not contacted on the day of the missed visit, the staff would send a message or call other contacts listed in the PIFS.
  4. During the first week of the visit window (from 14 days before the target date to 30 days after the target date), in addition to the reminders by telephone call or message, the staff contacted a peer or friend of the study participant to follow-up with participants. During weeks 2 through 6 of the visit window, staff would call all the listed telephone numbers or send messages once a week at various times. The locator data manager continued to update the contact log and locator information throughout the study period. Access to the PIFS was strictly protected through a database security system.
  5. Study staff made “locator contacts” with the participants at months 3 and 9. The locator contacts served the purpose of enhancing retention by providing a mechanism to confirm or update the participant's locator information, confirm or reschedule the participant's next follow-up visit, and reinforce instructions for the participant to contact the study site to update locator information and/or, if needed, request HIV counseling and/or testing between scheduled visits. The contacts were conducted in person at the study site or via telephone.
  6. Reimbursement for time and travel and privacy protection: Participants were reimbursed for time and travel at each follow-up visit. To be consistent with local norms, reimbursement amounts were $7 (about 50 Yuan Renminbi) for each follow-up visit. In addition, refreshments, 12 free condoms, and 1 free lubricant were provided at each visit to increase participants' affinity with the study. A voluntary physical examination was offered free of charge to each of the participants, with free treatment if syphilis, gonorrhea, or genital warts were diagnosed. By closely collaborating with local gay-oriented nongovernmental organizations, we carefully selected the interview clinic with the fewest visitors to ensure the privacy of the participants and easy accessibility by a variety of transportation routes.
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Data Collection

Questionnaire-based interviews were conducted on a one-on-one basis in a separate and private room of the district clinic. Trained health professionals conducted the interviews. Each study participant was assigned a unique and confidential identification code for the questionnaire and blood samples. Data collected included sociodemographic information (eg, age, ethnicity, education, residence, income, marital status, and housing status) and behavioral information [eg, self-identified sexual orientation, the number of male sex partners in the past 3 months, had sex with foreign male partners in the past 3 months, participated in male group sex in the past 3 months, had commercial sex with male partners in the past 3 months, were money boys (male sex workers), had unprotected anal intercourse with regular or casual male partners in the past month, had sex with female sex partners in the past 3 months, frequency of alcohol intoxication in the past 3 months, illicit drug use in the past 3 months, diagnosed with any STDs by a clinic physician in the past, received any AIDS-related services in the past 3 months, and received HIV testing in the past]. Blood samples were tested for all participants. Participants were instructed to return in 1 month to obtain results. Results were given anonymously using a preassigned unique code.

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Laboratory Tests

Blood samples were tested for HIV, HBV, HCV, and syphilis infections. The HIV infection status was determined by an enzyme immunoassay (Beijing Wantai Biological Medicine Company, Beijing, China) screening and an HIV-1/2 Western blot confirmation (HIV Blot 2.2 WB; Genelabs Diagnostics, Singapore). Hepatitis B surface antigen (HBsAg) was screened using an HBV enzyme-linked immunosorbent assay (Beijing Wantai Biological Medicine Company, China). Samples were tested for antibodies to HCV by enzyme-linked immunosorbent assay (Beijing Wantai Biological Medicine Company, China). Syphilis infection was determined using an enzyme immunoassay (Beijing Wantai Biological Production Company, Beijing, China) and confirmed using a passive particle agglutination test for Detection of Antibodies to Treponema pallidum (TPHA; OMEGA, Manchester, United Kingdom).

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Statistical Analysis

Questionnaire-based data and biological testing results were recorded, double checked, and compared with EpiData software (EpiData 3.0 for Windows; The EpiData Association, Odense, Denmark). After corrections, data were then converted and analyzed using statistical analysis system (SAS 9.1 for Windows; SAS Institute Inc, Cary, NC). The HIV, HBV, HCV, and syphilis incidence density rates were calculated based on Poisson distribution, with person-time of follow-up as the denominator. Categorical factors associated with retention were analyzed by the χ2 test, including baseline sociodemographic and behavioral characteristics. A multiple logistic regression model was constructed to select independent factors for retention after controlling for other potential confounding factors.

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Baseline Characteristics of the Participants

A total of 541 participants were screened. HIV prevalence was 4.8%; syphilis prevalence was 19.8%; HBsAg prevalence was 6.5%; and HCV prevalence was 0.4%. Of the 507 MSM who were HIV seronegative and eligible to enter the cohort, 93 (18.3%) had a syphilis infection, 24 (4.7%) were HBsAg positive, and 1 (0.2%) was HCV positive.

Of 507 participants, the median age was 26 years, with a range from 18 to 62 years; 91.9% belonged to the Han ethnic group; and 72.3% completed college or higher levels of education. Beijing residents accounted for 34.5%; the median monthly income was US $300; 67.1% were single, and 14.6% were married or cohabiting with female sex partners. Participants who identified as exclusively homosexual and predominantly homosexual accounted for 54.2% and 38.7%, respectively, whereas 7.1% of the participants were identified as predominantly heterosexual with only incidental homosexual activities. The median number of male partners in a lifetime was 10. In the past, 47.9% and 14.2% ever received an HIV test and any AIDS-related service, respectively; 30.8% had an STD diagnosed by clinic physicians. In the past 3 months, 72.6% of participants found male sex partners through the internet; 4.1% had sex with foreign male partners; 7.3% participated in male group sex; 6.3% had commercial sex with men, and 3.9% were money boys; 14.2% had sex with female partners; 21.1% drank alcohol ≥1 time per week in the past 3 months; and only 0.8% used illicit drugs (mainly ecstasy and ketamine). In the past month, 21.5% and 14.0% of the participants had unprotected anal intercourse with regular male partners and casual sex partners, respectively; 7.1% had unprotected sex with female partners (Table 1).



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Incident Infections of HIV, Syphilis, Hepatitis B and C Virus

Eleven HIV seroconversions were observed over 425.4 person-years of observation, 2.6 per 100 person-years (95% CI: 1.1 to 4.1) during the 12-month follow-up, with no statistically significant change during the 12 months of follow-up (incidence at 6-month visit = 1.3, 95% CI: 0 to 2.7; incidence at 12-month visit = 4.2, 95% CI: 1.3 to 7.1). Fifty-five syphilis seroconversions were observed over 325.8 person-years of observation; syphilis incidence was 16.9 per 100 person-years (95% CI: 12.4 to 21.3) during the 12-month follow-up period, with a statistically significant increase during the 12 months of follow-up (incidence at 6-month visit = 12.0, 95% CI: 7.0 to 15.4; incidence at 12-month visit = 23.3, 95% CI: 16.9-31.3). Thirteen HBV seroconversions were observed during the 12-month follow-up, 3.3 per 100 person-years (95% CI: 1.5 to 5.1), with no statistically significant change during the 12 months of follow-up (incidence at 6-month visit = 3.7, 95% CI: 2.7 to 6.2; incidence at 12-month visit = 2.8, 95% CI: 0.4 to 5.3). One HCV seroconversion was observed over the study period, 0.2 per 100 person-years (95% CI: 0 to 0.7).

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Predictors of Cohort Retention

Of the 507 participants, 86.2% (437) were retained in the cohort at the 12-month follow-up visit. Of the 70 participants lost to follow-up, 28.6% moved out of the area, 11.4% had no time to participate in the 12-month follow-up study, and 4.3% did not want to participate in the12-month follow-up study. Other reasons included changing their cell phone number (14.3%), changing their cell phone number and QQ (21.4%), changing their cell phone number and email address (11.4%), and changing their cell phone number, addresses for QQ or MSN, and e-mail (8.6%).

In univariate analyses, associations of 12-month retention with the sociodemographic and baseline behavioral characteristic variables were evaluated. Factors significantly associated with cohort retention were higher education, higher monthly income, exclusively homosexual sexual orientation, had commercial sex with men, ever received a test for HIV, and appeared at the 6-month follow-up visit (Table 2). Two factors significant in univariate analyses were entered into a multiple logistic regression model. Higher education (adjusted odds ratio = 1.94, 95% CI: 1.03 to 3.66; P = 0.0396) and appearing at the 6-month follow-up visit (adjusted odds ratio = 26.15, 95% CI: 13.44 to 50.89; P < 0.0001) were significantly associated with 12-month retention in the final model.





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This study found a high HIV incidence in 2007 (2.6 per 100 person-years; 95% CI: 1.1 to 4.1) among MSM in Beijing, China. This is similar to our previous findings of the incidence among this group in the same district in 2005 (2.9%, 95% CI: 0.8% to 5.0%) and 2006 (3.6%, 95% CI: 1.3% to 5.9%) estimated by the BED capture immunoassay (BED-CEIA) assay.26 This study also found a high incidence of syphilis and HBV infection and a low incidence of HCV. Our baseline survey showed a low level of HCV prevalence (0.4%), a moderate prevalence of HIV (4.8%) and HBsAg (6.5%) but a high prevalence of syphilis (19.8%) among MSM in Beijing.

Compared with the prevalence (3.2% for HIV and 11.2% for syphilis) found in our previous study conducted in 2005 in the same district,5 our baseline data indicated a possible rising prevalence of HIV and a dramatic rise in syphilis prevalence (P < 0.001) among this group. This is consistent with a study of 3 consecutive respondent-driven sampling surveys among Beijing's MSM.27 The present study also found that the incidence of HIV at the 12-month visit increased 3.3 times compared with the rate at the 6-month visit; the incidence of syphilis also statistically significantly increased during the 12-month follow-up (data not shown). These consistent findings from the present cohort study, BED-CEIA incidence estimation,26 and cross-sectional studies5,27 support that HIV spreads rapidly among MSM in Beijing. Although MSM do not contribute a large proportion of the HIV cases so far in China,3,28 the rising prevalence of HIV among MSM in Phnom Penn, Cambodia (8.9%), Bangkok, Thailand (28.3%); Andhra Pradesh, India (18.2%),29,30 and especially in Chongqing, China (10.8%),1 signals that HIV has been introduced into the sexual networks of MSM in China and that this group is facing a rapid spread of HIV.

The high incidence of serological markers of HBV also indicated that this group was at risk of transmitting the HBV. Hepatitis B among MSM should be an eminently preventable infection because an effective vaccine is available.31 Innovative means of reaching this group for vaccination are needed. These findings underlined the urgency for better-targeted intervention to control the HIV, syphilis, and HBV epidemics in this group.

The high prevalence of syphilis infection found in this study was consistent with the other reports among MSM populations in different cities; for example, 6.9% in 5 cities of Jiangsu Province, 13.5% in Shanghai, 10.5% in Guangzhou, and 19.1% in Shenzhen city.22-25 High prevalence of syphilis among MSM was consistent with the large number of MSM who were participating in sexual behaviors that place them at risk for syphilis and HIV infections.5,32 This study has failed to demonstrate the correlation between HIV and syphilis incident infections (data not shown) due to small sample size, epidemiological synergistic relationship between STDs, particularly between ulcerative diseases like syphilis and HIV infection that have been evidenced elsewhere,33 including our previous study.14 The high prevalence of syphilis among MSM suggested high prevalent risk behaviors which may signal a potential rapid spread of HIV infection among MSM in Beijing.

In this prospective cohort study of 507 HIV-seronegative MSM, 86.2% of the participants successfully completed the 12-month study. This is the first study in China to evaluate the retention rate for a prospective cohort of MSM. MSM are difficult to retain in a cohort and hard to reach through routine intervention programs because MSM behaviors are considered socially unacceptable and pressure against MSM is anticipated in many countries. HIV Network for Prevention Trials Vaccine Preparedness Study has successfully followed up with 88% of 3257 MSM participants in 6 US cities during an 18-month period.34 A slightly higher retention rate (91.5%) was reported in an Argentinean 12-month cohort,35 and a lower rate (77%) was reported in a 12-month cohort among the same population in Vancouver.36

In this study, risk behaviors were not found to be associated with retention. A high enrollment rate (99%) could be a reason for the relatively high retention rate. Appearing at the 6-month follow-up visit was found to be independently associated with 12-month retention, and we believe that the findings from this study provided important information for developing future long-term prevention studies among MSM. It implies that the short-term retention rate in a preparedness pilot study should predict the long-term follow-up rate in a cohort study.37 Having a higher level of education was another predictor for 12-month retention in this study.

The main reasons for loss of retention in the study cohort included changing cell phone numbers, email address, or the address of online communication. The field pilot test of the study indicated that participants were not willing to provide contact information, such as a telephone number, home and/or mailing address; outreach contacts are nearly impossible to follow up with the participants. Poorer retention of study participants with less education might be the result of lack of interest in HIV testing and counseling. Taking these factors into consideration, we developed a vigorous retention plan by collaborating with a gay-oriented nongovernmental AIDS volunteer group, including locator information managed by the PIFS; suitable reimbursement for the participants' time and transportation; and free treatment for STDs offered in a nonjudgmental, friendly, and private environment. Ineffectiveness of outreach indicated in this study is dramatically different when compared with studies conducted in Western countries,36 where outreach contacts were the major way to follow up with MSM. We also mainly utilized outreach contacts to successfully maintain a high retention of IDUs in our previous cohort study.36,37Although it is generally believed that MSM are difficult to retain in a prospective cohort study, we found a relatively high retention rate in Chinese MSM.

This study has several limitations. Participants were recruited using multiple methods, which did not guarantee that we reached all MSM in the community. Nonparticipants might have different risk behaviors and therefore have a different risk of HIV infection and a different rate of retention than the participants. In addition, those lost to follow-up have a different demographic profile (education). Selection bias might lead to overestimation or underestimation of the true seroconversion rate for HIV, syphilis, HBV, and HCV. Our group is seeking to continue the current MSM cohort with an improved research design and to steer future research efforts toward innovative interventions for MSM in China. We believe that the data will help guide public health planning, preventive measures, and clinical research planning and help mobilize local officials and nongovernmental organizations to control the rapid rise of HIV and other STDs among MSM.

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We would like to thank Ms. Meredith Bortz from Vanderbilt University for article assistance.

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China; hepatitis; HIV; men who have sex with men; prospective cohort study; syphilis

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