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Risk factors of HIV infection and prevalence of co-infections among men who have sex with men in Beijing, China

Zhang, Xiaoxia; Wang, Chena; Hengwei, Wanga; Li, Xinxub; Li, Donglianga; Ruan, Yuhuab; Zhang, Xiaoyanb; Shao, Yimingb

doi: 10.1097/01.aids.0000304697.39637.4c
Original papers

Objectives: To investigate risk factors related to HIV infection and the prevalence of selected infections, especially sexually transmitted infections (STI) among men who have sex with men (MSM).

Design: A cross-sectional study including questionnaire and blood sample collection.

Methods: Between January 2005 and December 2006, 753 MSM were recruited through the voluntary counselling and testing (VCT) clinic at the Chaoyang District Centers for Disease Control and Prevention in Beijing. Sera samples were collected and tested for HIV, syphilis, Chlamydia trachomatis, Ureaplasma urealyticum, Toxoplasma gondii, and hepatitis C virus (HCV). Statistical analyses were performed to identify factors related to HIV and STI, as well as other co-infections.

Results: The prevalence of HIV-1 infection among MSM attending the VCT clinic was 2.1%. Among all MSM, 7.0% had syphilis, 5.6% Chlamydia, 4.4% U. urealyticum, 2.5% T. gondii and 0.8% HCV (13.8% had one or more). Among HIV-negative MSM, 13.3% had one of these infections, whereas among HIV-positive MSM, 93.8% had serological evidence of one or more co-infections (P < 0.0001). Individuals with HIV infection were significantly more likely to have had more male sex partners or to report frequent receptive anal sex in the past 6 months.

Conclusion: Serological evidence of infection with any of five STI or HIV-relevant conditions was far higher in HIV-infected than HIV-uninfected MSM. Co-infection in HIV-positive men was most frequent with syphilis. Our data suggest that strategies for HIV/AIDS and STI prevention and control among MSM should be synchronized.

From the aChaoyang District Center for AIDS/STD Control and Prevention, Beijing 100021, China

bState Key Laboratory for Infectious Disease Prevention and Control, National Center for AIDS/STD Control and Prevention, China CDC, Beijing 100050, China.

Correspondence to Xiaoyan Zhang at the National Center for AIDS/STD Control and Prevention, China CDC, Beijing 100050, China. Tel: +86 10 87789398; fax: +86 10 87789386; e-mail:

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According to the 2006 report on reportable infectious diseases [1], the top five infections in China were tuberculosis, hepatitis, diarrhoea, syphilis, and gonorrhoea. These five diseases accounted for 85.6% of total reported cases. Morbidity and mortality from sexually transmitted infections (STI), including HIV/AIDS, syphilis and gonorrhoea, increased by 3.5 and 7.2%, respectively, compared with 2005. New HIV infections were estimated to be 70 000 cases, with more than 40% of them via sexual transmission [2].

Several studies have examined the effect of infection with STI on HIV infection and transmission. The presence of STI, particularly those with ulcers, facilitates the sexual transmission of HIV-1 because the epithelial and mucosal barriers are disrupted. Syphilis and urethritis have been associated with a decrease in CD4 cell counts and an increase in HIV-RNA levels, both of which later improved after treatment for syphilis [3,4]. Syphilis has also been associated with a decrease in CD4 cell counts and an increase in HIV-RNA levels, both of which later improved after treatment for syphilis [3]. It is well documented that an increased HIV-1 plasma viral load is correlated with an increased risk of sexual HIV transmission [5]. Gonococcal infection can also facilitate the transmission of HIV-1 [6,7], although few studies have examined the underlying mechanisms. Interestingly, lipooligosaccharide, a component of the gonococcal outer membrane, can induce innate immunity through the engagement of Toll-like receptor 4, and lipooligosaccharide-treated human primary macrophages develop resistance to new HIV infection as well as to HIV provirus by the induction of IFN-β and the subsequent activation of signal transducer and activator of transcription, in vitro [8]. It was reported that treatment of urethritis in HIV-1-infected men who have sex with men (MSM) not receiving antiretroviral therapy (ART) resulted in a reduction in semen plasma HIV-1 viral loads; without ART, semen plasma viral loads were approximately fivefold higher in those with urethritis compared with controls [4]. STI may thus enhance the HIV infectivity of men not receiving ART in the developed world.

A study on an Amsterdam cohort of young HIV-negative MSM (n = 8630), however, observed no increase in HIV incidence with increases in STI, namely syphilis and gonorrhea [9]. Several years of increasing STI among MSM without any change in estimated HIV incidence makes the relationship between STI incidence and HIV transmission a subject for further study in the population.

As a result of their engagement in high-risk behaviours, such as unprotected anal sex, MSM are vulnerable to infection by HIV and other STI [10–14]. A previous cross-sectional study (n = 526) conducted in Beijing in 2005 found that the infection rates of hepatitis C virus (HCV) and syphilis among MSM were 1.5 and 11.2%, respectively, and this increased significantly to 17.7 and 35.3% among those co-infected with HIV [15]. The CD4 cell counts were lower and HIV viral loads were significantly higher in HIV-positive MSM co-infected with HCV or syphilis. The infection rate and effect of other STI on HIV infection among MSM in Beijing has not been established. In this study, we conducted an investigation of HIV and other infections that could be diagnosed by serosurvey among MSM attending the voluntary counselling and testing (VCT) clinic at Chaoyang Centers for Disease Control and Prevention (CDC), Beijing, China.

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Materials and methods

The study was approved by the internal review board of the National Center for AIDS/STD Control and Prevention, China.

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Study subjects

MSM were recruited between January 2005 and December 2006 through a VCT clinic at Chaoyang District CDC in Beijing. The clinic is open to all visitors for HIV testing. Participants were initially screened against the eligibility criteria, which included: (i) age 18 years or older; (ii) Beijing resident; and (iii) any lifetime history of sex with other men. Men who were eligible and willing to participate in the study provided written informed consent and completed a 30-min questionnaire. The questionnaire asked for demographic information (age, education, employment, marital history) and information about their engagement in risky behaviours (number of sexual partners, sexual preferences, condom use, engagement in group sex, and self-reported history of STI). The questionnaire was administered by a trained interviewer.

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Sample collection

Samples of whole blood (5 ml) were collected in sterile ethylenediammine tetraacetic acid tubes. All samples were transferred to the laboratory for testing no more than 6 h after collection, to be tested for HIV, syphilis, Chlamydia trachomatis, Ureaplasma urealyticum, Toxoplasma gondii, and HCV. The STI were tested as the principal purpose of this work, but T. gondii and HCV were tested given the serious burden of disease represented by both among HIV-infected individuals.

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Sera testing

All assays were carried out according to the manufacturer's instructions. HIV was first tested by enzyme-linked immunoassay (ELISA) kits (Beijing Wantai, Beijing, China) and positive tests were confirmed by Western blot assay (HIV blot 2.2; Genelab Technologies, Inc., Singapore). Those with a confirmed positive HIV test result were also tested for their CD4 cell count and viral load (data not presented). Syphilis quick test kits (rapid plasma reagin; Beijing Jinhao, Beijing, China) were used to test for syphilis, and positive samples were confirmed by the Treponema pallidum haemagglutination test (Omega, England). C. trachomatis was tested using IgM and IgG assay kits (Shanghai B&C Co., Shanghai, China). U. urealyticum was tested using IgM and IgG assay kits (Shanghai B&C Co.). Toxoplasma was tested by ELISA (Haitai Biocompany, Guangdong, China). HCV was tested by ELISA (Beijing Yapei, Beijing, China). Serum samples were assayed in duplicate.

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Statistical analysis

Data were entered into a database using EpiData 3.0 software (EpiData Association Odense, Denmark) and statistical analyses were performed using SAS 9.1 (SAS Institute Inc., Cary, North Carolina, USA). Chi square tests were used to compare differences in demographic characteristics, sexual practices, and STI or other infections by HIV status.

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Demographic characteristics and sexual risks

Not all MSM in VCT clinics agreed to participate in this study. Those who refused (3.5%) to answer the questionnaire were excluded from the study. A total of 753 MSM (96.5% of those approached) were recruited into the study. The men ranged in age from 18 to 55 years (mean ± SD 26.1 ± 6.8; median 25). All were Beijing residents in the past 6 months, although 74.3% had migrated from other provinces. More than half (51.2%) were college educated or above, 34.9% had attended senior high school, and 13.9% received a junior high school education or below. Occupations included office worker in an international company (24.4%) or in a local company (7.3%), students (17.3%), service industry workers (7.7%), labourers (6.6%), small business owners (7.1%), government employees (1.8%), and others (8.3%). The remaining 9.5% were unemployed.

Most participants were single (70.5%), and 19.3% were cohabiting with their homosexual partners. Approximately 9.6% of MSM had married a woman; 4.2% were still married, whereas 3.0% were separated from their wives, and 2.4% had divorced. Self-reported sexual behaviours indicated that 58.9% exclusively had sex with men and the rest had sex with both men and women (29.8% preferred men and 11.3% preferred women). The number of lifetime sexual partners varied from one to 300 (median 10), and one to 100 (median three) in the past 6 months. MSM who had had 20 or fewer sexual partners accounted for 73.8%, 13.1% had had 21–40 partners, and 13.1% had had more than 40 partners. Over 90% of study subjects had engaged in both oral (91.7%) and anal sex (97.6%), and 12.7% of MSM had participated in group sex in the past 6 months. Most of the MSM would not use a condom for oral sex if they knew their sexual partner personally. Notably, 11.9% of MSM self-reported a history of STI.

Demographic data and sexual risk practices for HIV-positive and HIV-negative MSM are presented in Table 1. Compared with HIV-negative MSM, HIV-positive MSM were more likely to have had more than 10 male sex partners in their lifetime (P < 0.05), and were more than five times more likely to have had insertive anal sex with a male partner in the past 6 months (P < 0.05).

Table 1

Table 1

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Prevalence of HIV-1 and other infections

Laboratory test results are presented in Table 2. Sixteen men (2.1%) tested positive for HIV-1. A total of 104 participants (13.8%) had other infections: 8.1% with syphilis, 6.2% with C. trachomatis, 4.8% with U. urealyticum, 2.% with T. gondii, and 1.2% with HCV. Thirty-nine (5.2%) had at least two infections.

Table 2

Table 2

Of the 16 HIV-positive MSM, 15 (93.8%) were co-infected with an STI or another infection (T. gondii or HCV), higher than for HIV-negative MSM (P < 0.05). Five (31.3%) had at least two types of co-infections. The most frequent HIV co-infection was syphilis, 6.1% in HIV-negative men compared with 50% in HIV-positive men (P < 0.05). Multivariable logistic regression analysis demonstrated that having had more than 10 lifetime male sex partners (adjusted odds ratio 4.1; 95% confidence interval 1.3–12.8) was independently associated with HIV infection among MSM.

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According to a survey conducted in metropolitan areas of China [16], the estimated HIV-1 infection rate among MSM was over 1% in 2004. In Beijing, over 3% of MSM were found to be HIV positive [10,15]. One in five MSM was ignorant of his risk of HIV infection and more than two-thirds of respondents reported engaging in unprotected sex during the previous 6 months [11,17]. A longitudinal study in six US cities reported that risk factors for HIV acquisition in MSM (n = 4295) related to their number of sexual partners, occurrences of unprotected anal intercourse, and alcohol or drug use before sex [14]. Whereas MSM data are comparatively scarce in China, it appears that similar dynamics are extant.

In this study, 2.1% of MSM were identified as HIV positive, which was not significantly different to earlier cross-sectional studies [10,15]. Compared with individuals without HIV infection, individuals with HIV infection were significantly more likely to have more male sex partners in their lifetime and to have frequent receptive anal sexual intercourse in the past 6 months. Unprotected receptive anal sex increases the probability of mucosal membrane trauma, which also increases the chance of HIV transmission, suggesting that China continues to face the threat of expanded HIV transmission among MSM.

In Beijing, it was reported that most men older than 39 years had been married [11]. The self-reported sexual behaviours in this study indicated that approximately 41% of MSM had engaged in sex with women as well as men, which was much higher than a previously estimated nationwide rate of 24% [18]. This suggests that there is a potential risk of the spread of HIV-1 between men who have sex with men and to their heterosexual partners.

Several surveys conducted in Beijing in the early 2000s found that over 20% of MSM had experienced STI [12]. Infection point prevalence or range was as follows for major STI: gonorrhea 22–35%, Condyloma acuminata 15–26%, non-gonococcal urethritis 14–24%, syphilis 8.5–19.5%, C. trachomatis 12.6%, herpes simplex virus type 2-IgG 6.1%, and genital herpes 3–5%. An approximately similar STI infection rate was observed in our study, although different STI were studied; 5.2% of our sample had at least two infections. Fully 13.8% of MSM in our study had serological evidence of an STI: 8.1% syphilis, 6.2% C. trachomatis, and 4.8% U. urealyticum, comparable to the prevalence data reported in other studies [12], as well as our previous cross-sectional study (11.2% for syphilis) conducted in Beijing in 2005 [15]. The infection rate of T. gondii (2.8%) is the first to be reported among MSM in Beijing, so the prevalence of this infection in MSM should be followed up in future studies. The rate of HCV infection (1.2%) was similar to our previous survey result in a similar population (1.5%) [15].

In this study, all factors including risk behaviours were collected on the basis of self-reported data. Respondents may have hidden some factors related to risk behaviours because of the sensitive nature of the information. To increase the accuracy of the behavioural information collected, all interviews were conducted one-on-one in separate rooms at the VCT clinic to maximize the protection of a subject's privacy. In addition, the interviewers were well trained both by local CDC staff and by MSM volunteers to establish a reliable interactive relationship.

STI are associated with an increased risk of HIV infection and transmission. The high prevalence of STI among MSM in Beijing, especially the much higher co-infection rate of STI with HIV, urges the need for a focused surveillance, control, and treatment programme for STI in HIV-infected and HIV-at-risk individuals. Our data underscore the importance of continuing efforts to educate and inform MSM, especially those who are HIV infected, about the importance of safer sex.

Sponsorship: This study was supported by specialized funds from the Beijing Health Bureau for capacity enhancement of the HIV laboratory network, and epidemiological study and strategies for HIV co-infection control and prevention (grant no. 200601) from the Chinese Ministry of Health.

Conflicts of interest: None.

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chlamydia; hepatitis C virus; HIV; sexually transmitted infection; syphilis; toxoplasmosis; ureaplasma serology

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