Zou, Huachun MD, MS*; Wu, Zunyou MD, PhD*; Yu, Jianping MD†; Li, Min MD†; Ablimit, Muhtar MD‡; Li, Fan MD‡; Pang, Lin MD, MPH*; Juniper, Naomi MS*
In most developed countries, men who have sex with men (MSM) were the first group affected by HIV/AIDS and they still account for a large proportion of reported HIV/AIDS cases.1,2 China's HIV/AIDS epidemic has progressed differently with intravenous drug users and former commercial blood donors accounting for more than 62% of accumulated HIV/AIDS cases between 1985 and 2006.3 HIV transmission through blood transfusion has been stopped; and methadone maintenance treatment, needle exchange programs, and health education have helped reduce the spread of HIV among drug addicts in China.4,5 Studies indicated rapid rising rates of HIV infection among MSM in China. In 2005, MSM accounted for 7.3% of China's estimated 650,000 people living with HIV/AIDS, however, by 2007, this figure had increased to 12.2% of the estimated 700,000 HIV/AIDS cases.3 The proportion of MSM in reported cases of HIV/AIDS in the China national notifiable disease system has dramatically increased from 0.4% in 2005 to 3.3% in 2007.3,6
Various determinants increase the likelihood MSM have large numbers of multiple lifetime sexual partners and engage in high-risk sexual behaviors rendering them more vulnerable to HIV and sexually transmitted infections (STIs).7,8 If appropriate and effective actions are not taken, China may face a significant increase in HIV infection among MSM.
According to the China Internet Network Information Center, by September 2007, nearly 71 million urban adult males were using the internet.9 It is estimated that 10%-15% of adult males in China have had lifetime male/male sexual experiences including kissing, fondling, mutual masturbation, and oral and anal sex.10
MSM are increasingly using the internet to look for sex, and significant associations between internet sex-seeking and high-risk sexual behaviors have been reported.11-13 There are growing numbers of international studies indicating sexual intercourse with male partners met online increases HIV/STIs risk,12,14 however, the characteristics of Chinese men who have sex with men who use the internet (MSMUI) have not yet been well documented. The nature of the internet makes it an ideal venue for recruiting understudied, at-risk groups,14 such as Chinese MSM who might be less willing to respond to more conventional research approaches. To better understand MSMUI in China, we conducted a cross-sectional survey of 429 MSMUI in 2 cities in China in 2007.
Participants, Recruitment, and Fieldwork Sites
In this study, MSM refers to men who have already had, or intent to have, oral or anal sex with other men and if not specified, sexual partners refers to male sexual partners. For 2 weeks before survey commencement (June 11 to July 11 in Beijing; July 16 to August 17 in Urumqi) and during the survey, identical banners containing information concerning our study were placed on the main pages of a national gay website and a Beijing-based MSM volunteer website inviting MSM to participate in our study. Contact information was also posted on 3 major national gay partner-seeking websites and 1 Xinjiang-based gay online chat room for recruiting participants.
Qualified participants met the following criteria: (1) ever had or likely to have sex with a man; (2) 18 years or older; (3) accessed gay information on the internet in the 3 months before study commencement. All participants were invited to come to the 2 voluntary counseling and testing (VCT) centers between 6 pm and 10 pm local time during the survey period. To ensure cohort compliance with enrollment requirements, the survey designer and an MSM community member were present at the VCT centers to screen participants for the duration of the study.
The study was based off-line in 2 VCT site, 1 in Beijing Xicheng District Center for Disease Control and Prevention (CDC) in Beijing and 1 in Xinjiang Uighur Autonomus Region CDC in Urumqi (the capital city of Xinjiang Uighur Autonomous Region).
Consenting participants were interviewed face-to-face by trained interviewers. Qualified HIV/STI counselors gave HIV counseling and provided referrals for social support or medical services as needed. A 5 mL of intravenous blood sample was collected for HIV and syphilis testing. All participants who completed questionnaires received 50 Chinese yuan renminbi (RMB) (about US $7.5) and some small gifts (condoms, lubricant, MSM health booklet) for their participation. Participants were surveyed on their sociodemographic characteristics, internet use, and HIV-related risk behaviors.
Blood samples were tested for HIV antibody using an enzyme-linked immunosorbent assay (Bio-Merieux, Boxtel, Netherlands), and positive results were confirmed by a HIV-1/2 Western Blot (HIV Blot 2.2 WB, Genelabs Diagnostics, Cavendish, Singapore). Syphilis antibodies were screened by enzyme-linked immunosorbent assay (Shanghai Kehua Biologic Production Company, Shanghai, China). Reactive samples were confirmed by a passive particle agglutination test for detection of antibodies to Treponema pallidum (Serodia TPPA; Fuji-rebio Inc, Tokyo, Japan).
Trained investigators explained to participants the aim, process, benefits, and potential risks of study participation before obtaining informed consent. Participants were informed survey participation was anonymous and voluntary, and they had the right to discontinue participation at any time. Ethical approval was obtained from the institutional review board of the National Center for AIDS/STD Control and Prevention, China CDC, Beijing.
EpiData software (EpiData 3.0 for Windows; The EpiData Association, Odense, Denmark) was used to double enter and validate the data. Statistical Analysis System (SAS 9.1 for Windows; SAS Institute Inc, Cary, NC) was used to analyze the data. A χ2 test was performed to assess whether proportions of key indexes between MSMUI from the 2 locations had any statistically significant differences. Logistic regression analysis was performed to assess potential risk factors related to HIV infection.
A total of 429 MSMUI were recruited; of whom, 153 were recruited from responding to the banners, 176 from collected contact details posted online, and 70 were referred by friends who had participated in the study. Of the 429 participants, 420 provided a blood specimen (of the 9 who did not provide a blood specimen, 6 were hematophobic and 3 believed they had no risk for infection and thus refused to provide a sample) and 399 completed a questionnaire (30 participants went to the VCT clinics when investigators were not present, so they did not complete the questionnaire but provided a blood sample and basic sociodemographic information). HIV/syphilis infection rates were based on data of the 420 men who provided a blood specimen. Logistic regression of potential factors influencing HIV infection was based on data of the 390 men who both provided a blood specimen and completed a questionnaire. Other statistics were based on data of the 399 men who completed a questionnaire. χ2 tests showed that there were no significant differences in proportions of key indexes (age, χ2 = 0.95, P = 0.33; ethnicity, χ2 = 0.31, P = 0.58; HIV infection rate, χ2 = 0.29, P = 0.59) between samples from the 2 cities. Analysis was based on the data from the 2 cities combined together.
Most articipants were young, educated, never married, and identified as homosexual (Table 1). Infection rates of HIV, syphilis, and HIV/syphilis coinfection were 4.8% (20 of 420), 11.4% (48 of 420) and 1.7% (7 of 420), respectively. MSM who had a low education level (senior high school or less) had a higher HIV rate (11.2%) compared with those who had a high education level (having some college or above, HIV rate of 2.47%, P = 0.001). Local resident had a lower HIV infection (1.5%) compared with non-local resident (6.6%, P = 0.043).
Lifetime Sexual Behaviors
The median number of lifetime sex partners was 10 (range: 0-1000) (Table 2). Rates of condom use in the last oral, insertive, and receptive anal sex were 9.1% (35 of 385), 66.3% (220 of 332) and 60.4% (200 of 331), respectively. Nearly 40% of participants consistently used condoms in both insertive and receptive anal sex in the past 6 months. Nearly half (164 of 399) ever had sex with a female partner and 42.1% (69 of 164) used condoms in the last such sex. The average age of sexual debut was 21, and the average absolute duration between realization of sexual orientation and first sex with a male was 3 years. No statistical difference was found in any of sexual behavioral variables for HIV and/or syphilis infections.
Internet-Related Sexual Behaviors
The internet was the most popular venue to find sexual partners with 82.2% (328 of 399) using it, followed by cafés or bars (14.8%, 59 of 399), bath houses (14.3%, 57 of 399), and parks and toilets (13.3%, 53 of 399) (Table 3). 13.8% (55 of 399) did not use the internet to find sexual partners but did use more traditional venues. Fifteen participants did not respond and 1 had never had sex with a man. Among MSMUI who were 24 years or younger, 83.6% (143 of 171) used the internet to find sexual partners. The next most common venue used by this group was bars (19.9%, 34 of 171). Among MSMUI older than 24 years, 81.1% (185 of 228) used the internet to find sexual partners. The next most common venue used by this group was bath houses (19.7%, 45 of 228).
Almost all (382 of 399) had ever met a male cyber friend (initial contact made online) offline and (362 of 399) had ever had sex with a cyber friend, with 69.1% (257 of 362) having 1-10 sexual cyber friends and 29.0% (105 of 362) having 11 or more such partners. More than half (220 of 398) met their first male sexual partner online. Percentages of condom use in the last oral sex, insertive anal sex, and receptive anal sex with cyber friends were 7.2% (25 of 349), 69.6% (201 of 289), and 68.7% (202 of 294), respectively. Most (270 of 382) never inquired about the HIV infection status of a newly met cyber friend.
No statistical difference was found in any of internet-related sexual behavioral variables for HIV and/or syphilis infections.
Perception of HIV/STIs Risk, Condom Use, and HIV/STIs Testing
Nearly half (47.9%, 191 of 399) had ever tested for HIV, and 26.3% reported at least 1 type of lifetime STI. A majority (59.5%, 237 of 399) of participants still perceived themselves to be at no or little risk of HIV infection and 21.1% (84 of 399) could not define their perception of risk. Within the ≤24 age group, rates of constant condom use during insertive and receptive anal sex within the past 6 months, respectively, were 47.1% (33 of 70) and 46.1% (35 of 75) for those who perceived no or little risk of HIV infection, 17.6% (3 of 17) and 9.5% (2 of 21) for those who perceived high or very high risk of HIV infection, and 34.8% (8 of 23) and 16.7% (5 of 30) for those who could not define their level of risk.
Nearly all (94.2%, 180 of 191) who ever tested for HIV knew the result of their last test, however, more than half (59.4%, 237 of 399) believed they were at no or low risk for HIV. More than half (59.6%, 28 of 47) of the syphilis-positive MSM who completed the questionnaire reported no STIs. Among those reporting a history of HIV/STIs, after diagnosis, almost all (99.0%, 104 of 105) reported using at least 1 method to reduce transmission of HIV/STIs, of which 57.1% (60 of 105) reduced the number of sexual partners, 29.5% (31 of 105) decreased penetrative sexual behaviors, 83.8% (88 of 105) used condoms on a regular basis, and 37.1% (39 of 105) started to test for HIV.
Factors Influencing HIV Infection
Table 4 shows logistic regression analysis of risk factors for HIV infection. Being 24 years or younger [odds ratio (OR) = 2.85, 95% confidence interval (CI): 1.05 to 7.75], being syphilis positive (OR = 4.78, 95% CI: 1.68 to 13.58), having used saliva as a substitute for lubricant (OR = 8.03, 95% CI: 1.03 to 62.52), and having bleeding gums or oral ulcers during oral sex (OR = 3.17, 95% CI: 1.13 to 8.88) were associated with HIV infection. However, the number of male sexual partners (OR = 1.00, 95% CI: 0.995 to 1.01) and being circumcised (OR = 0.73, 95% CI: 0.19 to 2.81) were not associated with HIV infection.
MSMUI had a high level of education as nearly three quarters had an education of some college or more, this is similar to other studies surveying MSM via the internet in China.10,15 With nearly a quarter of the MSMUI in our sample being students, education campaigns targeting student MSM websites may be valuable in controlling HIV/syphilis infection among this subpopulation of MSMUI.
MSMUI in China tend to be younger than MSM samples recruited offline. The median age of this sample (25 years) was younger than noninternet samples.7,8,10 Younger MSMUI tend to engage in more high-risk sexual behaviors than older MSM16,17 and greater frequency of high-risk sexual behaviors is related to higher rates of HIV infection.18,19 This relative youth may have implications for HIV/syphilis infection as the results indicate MSMUI ≤24 years have a higher HIV infection rate than those >24 years. Reasons for this might be: (1) they are sexually active, (2) they lack awareness of the concept of self-protection while having sex, and (3) they are comparatively passive in their sexual contacts with older partners and thus are in a disadvantaged position to protect themselves. China may face a widespread HIV epidemic among young MSMUI without timely interventions targeting this population. As the internet can be used effectively to provide sex education to young people in China,20 websites targeting student MSMUI may be used to provide health and sexual information.
The internet has become an important venue for MSM in China to find sex partners.15 A possible reason for the popularity of the internet as a sex partner seeking venue is that it offers some anonymity, allowing them to make contact with other MSM or to find specific types of partners, without negative social consequences in a time-efficient manner.11,13,21 This may explain why the median number of lifetime sexual partners of MSMUI was higher than that of non-internet-using MSM in China with a similar median age.7,8,22 Public health efforts to communicate with MSMUI must use the internet as this population may not be reached by traditional outreach methods.
A study in 6 US cities found young MSM with a low-risk perception reported considerable high-risk behaviors.23 This study found within the ≤24 years group, rates of constant condom use during insertive and receptive anal sex within the past 6 months were considerably higher among those who perceived no or little risk of HIV infection than among those who perceived high or very high risk of HIV infection (47.1% and 46.7% vs. 17.6% and 9.7%). MSMUI might consider more condom use equals decreased risk and therefore perceive less risk when condoms are used more often.
A study in San Francisco showed MSM continued to engage in risky sexual behaviors when diagnosed STI negative.24 Most participants were unaware of their STIs status as nearly 60% of syphilis-positive MSMUI reported no STIs. There are significant barriers for MSM in China to receive timely STI diagnosis and treatment: the price for diagnosis and treatment of STIs is high; MSM experience discrimination from clinic doctors and nurses; it takes days to receive test results; and the quality of clinical laboratory testing is not high and physicians often misdiagnose STIs.25 MSM in our study craved trustworthy and effective gay-friendly STIs clinics where they can receive appropriate therapy at a reasonable price. They preferred a MSM community member with a medical and psychological background to provide online HIV/STI counseling. Efforts should be made to expand coverage of HIV/STIs testing among MSMUI so as to increase their awareness of their serostatus. This may also have the effect of encouraging safer sexual practices as almost all (99.0%, 104 of 105) participants who reported HIV/STIs history tried to use at least 1 way to avoid transmitting HIV/STIs to others.
Most MSM who use the internet are in urban areas as internet coverage in the countryside is still limited. Two-thirds of participants in out study were not local residents of the study cities. This confirms the results of a qualitative study conducted in Shanghai.9,26 Nonresident MSM in China have a higher rate of sexual risk behaviors and HIV/STIs infection than resident MSM,7,10,22 which our study confirms as 85.0% (17 of 20) of HIV carriers and 68.8% (33 of 48) of syphilis carriers were nonlocal residents. Nonresident MSM faced difficulties in maintaining long-term relationships partly due to economic instability and the lack of a private dwelling. This subgroup is in immediate need of psychological support and HIV/STIs services.
Although the sampling methods used avoid the shortcomings of traditional sampling methods and surveys completed online,2,12 they have their limitations. MSM who use the internet only represent a portion of the MSM population in China, and the results of our study can not be generalized to all MSM in China. The results may not be generalizable to MSMUI in all cities in China, as it is possible there are behavioral differences in different regions. In addition, internet-use behaviors change rapidly China, so the results may only be applicable to the study period. Participants may have confused the purposes of the research with the provision of clinical care as testing for HIV/Syphilis was provided, therefore, a representative sample of MSMUI may not have been obtained.
We found that MSMUI engage in high-risk sexual behaviors and have high infection rates of HIV/Syphilis. More efforts are needed to enhance HIV/STIs counseling, testing, and treatment services. Online counseling facilitated by scaled-up online public health campaigns might be an effective manner of benefiting this population.
The authors are grateful to health officials and MSM community members in Beijing and Urumqi who supported the study and to subjects who participated in the study.
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