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Oct 14, 2009 - Keywords HIV 4 Syphilis 4 Men who have sex with men 4. Respondent-driven sampling 4 Guangzhou 4 China. Introduction. With 33.2 million ...
AIDS Behav (2011) 15:1058–1066 DOI 10.1007/s10461-009-9619-x

ORIGINAL PAPER

Possible Increase in HIV and Syphilis Prevalence Among Men Who Have Sex with Men in Guangzhou, China: Results from a Respondent-Driven Sampling Survey Fei Zhong • Peng Lin • Huifang Xu • Ye Wang • Ming Wang Qun He • Lirui Fan • Yan Li • Fang Wen • Yingru Liang • H. Fisher Raymond • Jinkou Zhao



Published online: 14 October 2009 Ó Springer Science+Business Media, LLC 2009

Abstract A respondent-driven sampling survey was conducted to investigate HIV related serological and behavioral characteristics of men who have sex with men (MSM) in Guangzhou, China, and to identify associated factors potentially driving the epidemic. Respondent- Driven Sampling Analysis Tool and SPSS were used to generate adjusted estimates and to explore associated factors. Three hundred seventy-nine eligible participants were recruited. The adjusted prevalence of HIV and current syphilis infection are 5.2% and 17.5% respectively. 60.3% have unprotected anal sex in the past 6 months. Unprotected anal sex, having receptive anal sex and current syphilis infection are significant factors associated with HIV infection. The potential for a rapid rise of HIV and syphilis infections among MSM in Guangzhou exists.

Fei Zhong and Peng Lin contributed equally to this paper. F. Zhong  H. Xu  M. Wang  L. Fan  F. Wen  Y. Liang Guangzhou Municipal Center for Disease Control and Prevention, 510080 Guangzhou, China P. Lin  Y. Wang  Q. He  Y. Li Guangdong Provincial Center for Disease Control and Prevention, 510300 Guangzhou, China H. Fisher Raymond San Francisco Department of Public Health, San Francisco, CA 94102-6033, USA J. Zhao Bill & Melinda Gates Foundation, Beijing Representative Office, 100027 Beijing, China J. Zhao (&) Ping’an International Financial Center, 1901 Tower B, No. 1–3 Xinyuan South Road, 100027 Beijing, Chaoyang District, China e-mail: [email protected]

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Targeted interventions with voluntary counseling and testing (VCT) and sexually transmitted infection (STI) services are needed to address the epidemic, with a focus on such subgroups as those of with current syphilis, and non-official Guangzhou residence status. Keywords HIV  Syphilis  Men who have sex with men  Respondent-driven sampling  Guangzhou  China

Introduction With 33.2 million people worldwide currently infected, and with 2.1 million deaths in 2007 alone, the HIV pandemic is one of the most significant public health challenges of the twenty-first century [1]. In China, the HIV epidemic is driven by sub-populations who are at the highest risk for acquiring or transmitting HIV, such as injecting drug users (IDU) and men who have sex with men (MSM) [2]. In recent years, the predominant route of transmission has shifted from blood exchange (e.g. IDU) to sexual behavior in China [3]. Some studies have reported the rapid increase of HIV prevalence among MSM in Asia in recent years, from 17.3 to 28.3% between 2003 and 2005 in Bangkok, Thailand [4, 5], 18.9% in Pune, India [6], and from 0.4 to 5.2% between 2004 and 2006 in Beijing, China [7]. Because of the stigmatization of homosexuality in contemporary China, social taboos and discrimination lead MSM to be discreet about their sexual behavior and thus are hard-to-reach [8, 9]. Most studies of MSM in China recruited participants by convenience sampling from key volunteers or venues [10–13]. Convenience sampling may miss some sub-groups that are hidden and not easily accessed, and does not lend itself to achieving a diverse sample. Respondent-driven sampling (RDS), a relatively

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new sampling method, has been adopted by public health researchers as a promising alternative means to sample most-at-risk populations for biological and behavioral HIV surveys [14]. One of the advantages of RDS over other methods of sampling hidden populations, such as timelocation sampling, is that it requires little in-depth formative research among study populations and can acquire a quasi-probability sample [14]. RDS has already been used worldwide for sampling IDU, MSM, and commercial sex workers (CSW) successfully [14–16], and was recommend by Center for Disease Control and Prevention (CDC) as one of sampling approaches for National HIV Behavioral Surveillance in US [17]. Guangzhou is the capital city of Guangdong, a southern province in mainland China, and is remarkable for its rapid economic growth. With a relatively tolerant multicultural environment, job opportunities, as well as a large population of men [18], Guangzhou attracts MSM from all over the country. Two studies among MSM in 2003 (n = 121) and 2004 (n = 201) reported two and zero HIV infections from convenience samples, respectively [13, 19], while HIV prevalence in Guangzhou was also documented at 1.3% in 2006 from a sample of 423 MSM through longchain referral recruitment [20], with current syphilis infection rising from 2.0 to 3.8% between 2004 and 2006, indicating the possible increase in HIV infection among MSM. To investigate the possible trend of HIV related serological and behavioral characteristics of MSM in the city, a special study was conducted using RDS. An additional aim of the study was to identify potential risk factors driving the HIV epidemic among MSM.

Methods

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Sampling Method and Participant Recruitment RDS was used to recruit the study participants. The theories underlying RDS hypothesize that the socio-demographic characteristics of the seeds have no significant impact on the final sample composition [21, 22]. However, ideally seeds should be diverse based on demographic and other key variables to improve the chances of reaching equilibrium at a faster rate [21, 22]. The number of seeds selected for a particular sample size is still being tested. Research experience indicates that somewhere between 6 and 20 seeds is adequate depending on the study sample size [14]. In this study, a total of 13 diverse seeds were selected: five were older than age 30; seven were college educated; and by venue where they typically meet sexual partners, one from pubs, three from parks, and nine from the internet. These seeds had large social network sizes and were well connected to other members of the target population. All these seeds were selected on the basis of recommendations by leaders of MSM community. Each seed was given three coded coupons, which were valid for 1 month, to recruit his peers. Persons who presented with a valid coupon and who were eligible were consented, enrolled, and, in turn, given three recruitment coupons to give to their peers. Recruitment continued until equilibrium was achieved on key variables which were tracked during the progress of the study. A primary incentive, including a gift (worth about 2 US dollars) and 20 Yuan cash (approximately 3 US dollars), was given for participation in the interview and the provision of 5 ml blood for serological testing. A secondary incentive, 10 Yuan cash (approximately 1.5 US dollars) was given for every additional recruitment of MSM peers. For each participant participating in the study, pre- and post-test counseling were provided. Referral services were provided to HIV or syphilis positive cases.

Participants Measures The population of interest for this study was men who had anal or oral sex with men in the past 12 months and who resided in Guangzhou for longer than 3 months at the time the study was conducted. Participants were also 18 years old or greater and had participated in the study for the first time. The study was conducted at the HIV voluntary counseling and testing (VCT) clinic of Guangzhou CDC, which is located downtown and with convenient public transportation. All study procedures were introduced to participants by staff. Written informed consent was obtained from each of the participants prior to completing the questionnaire and blood draw. The study protocol was developed and approved by the National Center for AIDS/ STD Prevention and Control (NCAIDS), China CDC, which included human subjects’ approval.

After eligibility screening and informed consent, each participant provided 5 ml intravenous blood prior to an anonymous face-to-face questionnaire interview in a private room. Items included in the questionnaire were demographic information, knowledge and attitudes about HIV/AIDS, access to HIV prevention services, sexual behavior with men and women, drug use, and sexually transmitted infection (STI) symptoms and treatment. Specimens were tested for HIV antibody and syphilis antibody. HIV screening was conducted by using two enzyme-linked immunoassays (ELISAs; Diagnostic Kit for Antibody to Human Immunodeficiency Virus, BioMe´rieux, Boxtel, The Netherlands, Lot NO: A58LB; Beijing BGIGBI Biotech, Beijing, China, Lot NO: 20071201). If the

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result of one ELISA was positive, a Western Blot test was conducted for confirmation (MP Biomedicals Asia Pacific Pte Ltd, Singapore, Lot NO: AE8021). Syphilis screening was performed by rapid plasma regain (RPR; Shanghai Kehua Bioengineering Co. Ltd, Shanghai, China, Lot NO: 20080110). Specimens testing positive for syphilis antibody were confirmed by the treponema pallidum particle agglutination test (TPPA; Livzon Group Reagent Factory, Zhuhai, China, Lot NO: VN71109) to assess current infection. Statistical Analysis Data were double entered, and consistency tested using EpiData (version 3.1, Denmark). After data cleaning, Respondent-Driven Sampling Analysis Tool (RDSAT, version 5.6.0, available free at www.respondentdriven sampling.org.) was used to generate adjusted point estimates and 95% confidence intervals (95% CI). This was achieved by adjusting for the sizes of participants’ social networks and individual recruitment patterns [22]. Estimates of network size were based on self-report in response to this question: ‘‘In this city, how many MSM do you know? That is, you know the person’s face and name/ nickname, have his contact information, and could get in touch with him within the next 30 days’’. Since RDSAT could not perform multivariate analysis, SPSS (version 11.5, LEAD Technologies Inc.) was used to perform univariate and multivariate analysis after assigning cases individual weights for HIV and syphilis infection which were exported from RDSAT. The factors associated with HIV infection and current syphilis infection were assessed using univariate logistic regression models, then multivariate logistic regression models. There were eight core questions to evaluate AIDS awareness. AIDS awareness was defined as the rate of correctly answering six or more out of the eight core questions [23]. Coverage of prevention services was defined as receiving any services including condom distribution, lubricant distribution, peer education, STI diagnosis or treatment, HIV counseling or testing, or AIDS/STI educational materials in the past year. No risky anal sex was defined as no anal sex in the past 6 months or consistent use of condoms during anal sex with men, any other responses were coded as unprotected anal intercourse (UAI). No risky vaginal sex was defined as no vaginal sex in the past 6 months or consistent use of condoms during vaginal sex with women, any other responses were coded as unprotected vaginal intercourse (UVI). Unordered categorical variables, such as venues where participants usually meet sexual partners, were entered into the logistic model as dummy variables. Odds ratio (OR) and 95% CI were calculated in the multiple logistic regression model

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using a conditional backward elimination and stepwise method.

Results The study started on 4th May, 2008, and was completed on 31st August, 2008. A total of 956 coupons were distributed with 386 (40.4%, including seeds) being returned. Seven participants were referred to the VCT clinic due to ineligible conditions (i.e. one was younger than 18 years old and six did not report any anal or oral sex with men in the past 12 months). All 379 eligible participants completed the questionnaire and provided blood samples. All participants with positive HIV or syphilis results were provided with post-test counseling and referred to appropriate treatment and care services. Procedure diagram depicting the RDS recruitment among the 379 MSM can be seen in Fig. 1. Equilibrium was achieved by wave 11 with regard to age, marital status, hukou (official residence status), educational level, venue where they typically meet sexual partners, and current syphilis infection rate. Recruitment continued to the 14th wave. Serological and Demographic Characteristics The adjusted prevalence of HIV is 5.2% (95% CI: 2.1– 8.4%), 17.5% (95% CI: 13.6–21.5%) for current syphilis, and 3.2% (95% CI: 1.0–7.2%) for HIV and current syphilis co-infection. Table 1 shows point estimates and 95% CIs for demographic characteristics in this study. Less than a quarter (21.3%) of MSM has Guangzhou hukou. About half (50.3%) are younger than 30 years old, with age range from 18 to 51 years old. Most (51.1%) are single, 21.5% are currently married, 15.3% are living with male/female partners, and 12.1% are divorced or widowed. 45.0% have college or higher education. HIV Related Behaviors, AIDS Awareness and Access to Prevention Services HIV related sexual behaviors, HIV/AIDS knowledge awareness, access to HIV prevention services, and self reported STI signs or symptoms can be seen from Table 1. The majority (90.3%) of MSM have a high level of knowledge about AIDS prevention. About three quarters (73.5%) access at least one AIDS prevention service in the past 12 months. Only 14.3% received an HIV test in the past 12 months and all knew their test results. In this study, 19 HIV positive MSM were detected. Two of them have taken an HIV test in the past 12 months; however, the results of their previous test were negative.

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Fig. 1 Diagram of RDS sampling procedure among MSM (n = 379) in Guangzhou, 2008

The majority of MSM report being either homosexual (52.5%) or bisexual (33.9%). Two-thirds (68.0%) of MSM typically meet their partners through the internet, and 11.7% in parks or public lawns. 12.0% have no male partners, 29.4% have one, and 58.7% have two or more male partners in the past 6 months. 29.2% of MSM are insertive, 18.5% are receptive, and 52.3% are both insertive and receptive during anal sex. As for female partners, 71.7% have none, 26.1% have one, and 2.2% have two or more. 60.3% of MSM have UAI, 19.0% have UVI, and 10.4% have both UAI and UVI in the past 6 months. About one-fifth (19.9%) have signs or symptoms of STI in the past 12 months, 31.9% of MSM buy medications on their own and 30.1% do nothing about these symptoms. Only a few report commercial sexual behaviors or drug use, 3.7% buy sex from any man, 0.7% sell sex to men, and 1.7% use illicit drugs. HIV and Current Syphilis by Demographic, Behavioral and Serological Factors Factors associated with HIV or current syphilis infection by bivariate analysis can be seen in Table 2. UAI (being insertive or receptive) and current syphilis infection are significant factors related to HIV infection. MSM who have unprotected anal sex in the past 6 months, who are the receptive partner during anal sex, or have a current syphilis infection, have a significantly higher prevalence of HIV. As for factors associated with current syphilis infection,

educational level, venue for meeting partners or HIV infection are significantly associated with syphilis infection. MSM who have a lower educational level, report always meeting partners in pubs or parks, or have an HIV infection, have higher prevalence of current syphilis. AIDS awareness, coverage of AIDS prevention services, and receiving an HIV test in the past 12 months are found to be protective factors for HIV or current syphilis infection, although they are not statistically significant. In addition, there was no significant difference in condom use between those who received any prevention service and those who received no prevention services in the past 12 months (P = 0.765), or between those with an HIV testing history and those without (P = 0.781; data not tabulated). Predictors for HIV and Current Syphilis Table 3 shows the results of multivariable logistic regression of data from MSM who were infected with HIV or current syphilis, respectively. UAI (being insertive or receptive) and current syphilis infection are strongly associated with HIV infection. The risk of HIV infection is 5.1 times higher among MSM who had unprotected anal sex (OR = 5.1, 95% CI: 1.3–19.8) than those who did not, after adjusting for age, education level, hukou, marital status, venue for meeting partners, receiving an HIV test in the past, AIDS awareness, coverage of AIDS prevention services, and number of partners. The risk of HIV infection is 6.2 times higher among MSM who are the receptive

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1062 Table 1 Demographic characteristics and HIV related behaviors of MSM in Guangzhou, China (n = 379)

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Characteristics

Crude % (N)

Adjusted % (95% CI)

Official Guangzhou residence status

23.0 (87)

21.3 (17.9–26.8)

4.6 (18)

4.8 (2.4–7.3)

Unemployed Age group \20

1.0 (4)

1.1 (0.4–1.8)

20–

49.7 (189)

49.2 (42.4–56.6)

30–

35.7 (135)

36.8 (30.7–42.6)

40–

13.5 (51)

12.9 (8.5–17.5)

Marital status Single

50.9 (193)

51.1 (44.7–57.6)

Married

22.0 (83)

21.5 (16.3–26.9)

Living with male partner

14.2 (54)

14.5 (11.0–18.3))

Living with female partner Divorced or widowed

0.8 (3)

0.8 (0.0–2.1)

12.1 (46)

12.1 (8.2–16.3)

22.3 (85) 30.2 (114)

24.5 (17.9–31.2) 30.5 (25.1–35.6)

Education level Junior high school or lower Senior high school, technical

47.5 (180)

45.0 (37.9–52.8)

AIDS awareness

College or higher

90.7 (344)

90.3 (86.6–93.7)

Coverage of AIDS prevention services

74.7 (282)

73.5 (68.7–78.5)

HIV test in the past 12 months

14.8 (56)

14.3 (10.7–18.5)

Homosexual

53.2 (202)

52.5 (46.7–58.6)

Bisexual

34.0 (129)

33.9 (28.8–39.7)

Sexual orientation

Heterosexual

0.7 (2)

0.8 (0.0–1.9)

12.1 (46)

12.7 (9.1–16.2)

Pub, disco, tearoom, or club

6.4 (24)

5.9 (3.4–8.8)

Spa, bathhouse, or massage

9.0 (34)

8.9 (5.2–12.9)

Park, public toilet, or public lawn

13.7 (52)

11.7 (7.6–14.8)

Internet

65.1 (247)

68.0 (60.9–75.3)

5.9 (22)

5.5 (3.3–8.8)

0

11.8 (45)

12.0 (8.2–15.8)

1

29.7 (112)

29.4 (24.3–35.2)

2

21.7 (82)

22.4 (17.7–27.2)

3–

36.9 (140)

36.2 (31.1–41.5)

Not sure Venue for meeting partners

Other Number of male partners

Role of anal sexa CI confidence interval, UAI unprotected anal intercourse, UVI unprotected vaginal intercourse, STI sexually transmitted infection a

The denominator is the number of MSM who had anal sex in the past 6 months

Insertive

30.6 (102)

29.2 (23.7–35.7)

Receptive

19.0 (63)

18.5 (13.7–22.8)

50.4 (168)

52.3 (45.9–58.8)

UAI

Both

60.9 (231)

60.3 (55.4–66.2)

UVI

19.0 (72)

19.0 (14.4–24.2)

Symptoms of STI in the past 12 months

19.7 (75)

19.9 (15.7–24.2)

partner during anal sex than among those who are insertive. Current syphilis infection is independently related to HIV infection (OR = 8.3, 95% CI: 2.3–30.6). In Table 3, hukou, marital status, venue for meeting partners, receiving an HIV test in the past 12 months, and

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HIV infection are independently related to current syphilis infection, after adjusting for other factors. Being an official Guangzhou resident is a protective factor for having current syphilis infection (OR = 0.3, 95% CI: 0.1–0.9). The risk of syphilis infection among MSM who are married,

AIDS Behav (2011) 15:1058–1066 Table 2 Factors associated with HIV-seropositivity and current syphilis infection among MSM in Guangzhou, China

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Factors

HIV-seropositivity

Current syphilis infection

Adjusted % (95% CI) P

Adjusted % (95% CI) P

Marital status

0.389

Single Married Living with male partner

0.093

4.2 (1.2–6.8)

13.3 (9.2–18.6)

3.3 (0.1–6.8)

24.5 (13.4–34.4)

11.7 (2.1–22.9)

20.6 (11.7–30.8)

Living with female partner

7.6 (0.0–50.0)

Divorced or widowed

6.3 (0.0–14.1)

Education level

84.2 (–)a 17.2 (7.3–31.2) 0.328

Junior high school or lower

7.7 (1.9–14.7)

28.7 (19.2–37.8)

Senior high school, technical

6.1 (1.9–11.8)

26.2 (17.4–34.3)

College or higher

2.7 (0.0–6.2)

8.4 (5.3–13.7)

\0.001

1.1 (–)a

44.4 (21.1–66.5)

\0.001

Spa, bathhouse, or foot/body massage

0.9 (0.0–2.5)

23.8 (9.7–40.8)

0.061

Park, public toilet, or public lawn

4.3 (0.0–9.9)

26.6 (11.6–34.5)

0.004

Internet

6.7 (2.4–11.0)

12.2 (8.7–17.0)



Venue for meeting partners Pub, disco, tearoom, or club

Other

a

1.2 (–)

23.2 (0.3–45.2) 0.025

7.2 (2.7–11.7)

15.9 (11.5–20.9)

No

1.5 (0.0–3.6)

19.0 (11.9–25.1)

Role of anal sex

0.484

Insertive

4.7 (0.0–13.0)

Receptive

11.2 (2.9–19.3) 2.7 (0.3–5.8)

HIV-seropositive CI confidence interval, UAI unprotected anal intercourse a

RDSAT failed to generate 95% CI since the number of some subgroups was quite few

No Current syphilis infection



15.4 (8.1–22.5)

0.038 14.6 (7.1–25.7) 0.563 17.8 (11.3–23.7) –

0.011



57.3 (30.5–88.3)



15.9 (11.9–19.3) 0.010



Yes

17.7 (6.1–35.5)



No

2.9 (0.6–4.9)



living with partners (either male or female), or divorced, is higher than among single MSM. Receiving an HIV test is a protective factor (OR = 0.3, 95% CI: 0.1–0.9).

Discussion In this study, HIV prevalence in 2008 is estimated at 5.2% among MSM in Guangzhou, which is greatly higher than 0 in 2004 and 1.3% in 2006 [13, 20]. Supporting this possible rise is the accompanying increase in the high rate of current syphilis infection (from 2% in 2004 to 17.5% in 2008) and unprotected anal sex (from 54.7% in 2004 to 60.3% in 2008) [13], and increased prevalence of HIV and current syphilis in other cities in China [7, 24]. Unprotected anal sex, current syphilis infection, and receptive role during anal sex are significant factors

0.359 0.425

Yes

Yes

0.865

0.745

UAI

Both



associated with HIV infection among MSM in Guangzhou. Previous results from 2004, particularly the overall high unprotected anal sex [13], also support these findings. In Bangkok, HIV prevalence among MSM rose from 17% in 2003 to 28% in 2005, and it was estimated that as many as one in five (21%) new HIV infections in Thailand during 2005 were attributable to unprotected sex between men [4]. In China’s more recent epidemic, it has been estimated that up to 7% of HIV infections might be attributable to unprotected sex between men [25]. In this study, the risk of HIV infection was found to be 5.1 times higher among those engaging in unprotected anal sex with nearly twothirds of MSM still engaging in this behavior, implying a potential for further expansion of the HIV epidemic among MSM in Guangzhou. Furthermore, the risk of acquiring HIV among MSM with current syphilis infection is 8.3 times higher than

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Table 3 Factors associated with HIV-seropositivity and current syphilis infection by multivariate logistic regression analysis, among MSM in Guangzhou, China

b

Factors

AOR

95% CI

Wald Chi Sq

HIV-seropositivity UAI

1.6

5.1

1.3–19.8

5.5 

Role of anal sex Insertive

1.0



Receptive

1.5

6.2

1.3–29.4

Both

0.3

2.0

0.4–9.8

0.2

1.8

8.3

2.3–30.6

10.7  

-1.5

0.3

0.1–0.9

4.3 

Current syphilis infection

– 4.7 

Current syphilis infection Official Guangzhou residence status Marital status Single

1.0



Married

4.9

6.1

1.4–26.3

8.3 

Living with male partner

4.8

8.1

1.7–38.5

8.2 

Living with female partner

4.4

4.9

1.2–19.2

6.7 

5.1

125.0

4.1–1,000.0

9.0  

Divorced or widowed Venue for meeting partners Internet

AOR adjusted odds ratio, CI confidence interval, UAI unprotected anal intercourse  

P B 0.05;

  

P B 0.001

1.0



Pub, disco, tearoom, or club

1.5

5.2

1.3–21.6

4.6 

Spa, bathhouse, or foot/body massage

1.3

3.8

1.1–13.2

4.1 

Park, public toilet, or public lawn

1.4

7.5

1.2–46.6

4.2 

Other

1.7

7.3

2.6–20.6

9.8  

-1.3

0.3

0.1–0.9

4.0 

1.7

6.7

2.1–21.5

10.0  

HIV test in the past 12 months HIV-seropositivity

those who without syphilis. Current syphilis infection can be viewed as a marker for high-risk sexual practices, such as unprotected sex and/or multiple partners. Furthermore, STIs can enhance the acquisition of HIV [26, 27]. The presence of untreated sexually transmitted diseases, such as syphilis, gonorrhea, and chlamydia, can also greatly increase the risk of HIV transmission. Another important finding is the high prevalence of current syphilis. Through multivariate analysis, hukou, marital status, venue for meeting partners, history of HIV testing, and HIV infection are significantly and independently associated with current syphilis infection. MSM who are migrants or usually meet partner in pubs, spas, or parks may have higher risk for current syphilis infection, implying that these subgroups need more services and interventions, such as promotion of condom use and HIV/STI counseling and testing services. Receiving an HIV test is a protective factor for syphilis transmission, demonstrating that promotion of VCT may help to stop the expansion of STI and HIV infection. According to the results of bivariate analysis, AIDS awareness, coverage of AIDS prevention services, or VCT may also help to reduce the rise of HIV prevalence. It has also been demonstrated by many studies that increasing awareness of HIV status through accessible

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AIDS prevention services may reduce HIV transmission [28–31]. High current syphilis prevalence was found among MSM with low educational attainment. Additionally, this subgroup has significantly higher rate of unprotected vaginal sex than those with higher educational attainment. They have unprotected sex with female partners and thus may serve as potential epidemiological bridge for HIV/STI to their female partners. In addition to unprotected sexual practices, another associated factor is that a majority of MSM have two or more male partners. It is even more worrisome that nearly two-thirds of MSM with STI symptoms did not seek proper treatment for those symptoms. Overall HIV testing was low. Adoption of safer behaviors has not been commensurate with increased HIV/AIDS knowledge. Although RDS has apparent advantages in reaching diverse segments of MSM populations, it has still a number of limitations. Tracking refusal rates and the potential impact of non response bias is still being investigated [22]. Secondly, non-random recruitment of peers could influence the estimates in unknown ways [22]. As in other cross-sectional surveys, the study is also prone to a number of limitations. Firstly, a cross-sectional study cannot prove the causative relationship between

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behavioral exposure and HIV or syphilis infection. A cohort study can be designed and implemented to examine whether the associated factors in this study are risk/protective factors. Secondly, fewer MSM reported having commercial sex with men and using illicit drug than in 2006 [20]. The more sensitive nature of commercial sex and the illegal nature of drug use may underestimate the actual rates of commercial sex and drug use as participants may be reluctant to disclose these behaviors. With these limitations in mind these data should be cautiously interpreted. In conclusion, the results of this study suggest a possible rapid raise of HIV and current syphilis infections among MSM in Guangzhou. Unprotected anal sex, being the receptive partner during anal sex and current syphilis infection are associated with HIV infection, whereas receiving VCT may reduce the risk of current syphilis infection. Targeted interventions with VCT and STI services are needed to address the epidemic with a focus on such subgroups as those with current syphilis, non-official Guangzhou residence status, low educational level, and who are married or divorced.

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8. 9.

10.

11.

12.

13.

14.

15. Acknowledgments We would like to thank the Bill & Melinda Gates Foundation (Grant 49277) for funding this study. We feel indebted to MSM volunteers and venue owners who help the mobilization and organization efforts during the field surveys and participants who voluntarily participated. We also want to thank staff of Section of AIDS Control and Prevention, Guangzhou Center for Disease Control and Prevention, for their excellent work on this study.

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