Prevalence of syphilis infection and associations with sexual risk behaviours among HIV-positive men who have sex with men in Shanghai,China

Abstract

The aims of this study were to understand the prevalence and correlates of syphilis infection among HIV-positive men who have sex with men (MSM) in Shanghai, China. A total of 200 HIV-positive MSM participants were recruited using “snowball” sampling. Participants were tested for syphilis and completed a one-time questionnaire which included demographic characteristics, sexual behaviours with male and female sexual partners, substance use, and use of antiretroviral medications. Prevalence of syphilis infection was 16.5%. Among HIV/syphilis co-infected participants, 63.6% reported having anal sex with male partners and 24.2% did not use condoms consistently during the past six months; 66.7% reported having oral sex with male partners and 51.5% reported unprotected oral sex during the past six months. Factors associated with testing seropositive for syphilis infection included receptive anal sex with a male partner in the past six months (AOR = 12.61, 90% CI = 2.38–66.89), illicit drug use in the past six months (AOR = 11.47, 90% CI = 2.47–53.45), and use of antiretroviral medication (AOR = 4.48, 90% CI = 1.43–14.05). These data indicate a need for “positive prevention” interventions targeting HIV-positive MSM in China.

Keywords

HIV AIDS sexually transmitted infections syphilis men who have sex with men MSM China risk behaviour

Introduction

HIV prevalence among men who have sex with men (MSM) in China has been rapidly increasing in recent years such that sexual transmission between men has now become an important mode of HIV transmission in China.^1–4 Concurrent with increases in HIV incidence and prevalence, syphilis rates have also been on the rise among MSM populations in China. A recent meta-analysis on co-infection of HIV and syphilis among MSM in China found that the syphilis prevalence among Chinese MSM nearly doubled from 6.8% in 2003–2004 to 13.5% in 2007–2008; the HIV/syphilis co-infection prevalence also nearly doubled from 1.4% to 2.7% between 2005–2006 and 2007–2008.⁵ Another meta-analysis of surveys conducted in China between 2001 and 2008 estimated an overall 9.1% prevalence of syphilis among MSM in China.⁶

HIV and syphilis share a common mode of transmission. Thus, the interaction between HIV and syphilis is of importance in both sentinel surveillance and clinical treatment of both infections. Among MSM populations, HIV infection has been shown to be strongly associated with syphilis infection.^7,8 A large body of research conducted internationally among MSM suggests that the prevalence of HIV and syphilis co-infection may be as high as 20% in some MSM populations.^9–11 In U.S. settings, the prevalence of HIV infection has been shown to be two-to-three times higher among MSM who are co-infected with syphilis compared with MSM not infected with syphilis.¹² In addition, syphilis outbreaks have occurred in large cities in Italy where syphilis infection was more prevalent in HIV-infected MSM.^13,14 A study conducted in Amsterdam found a significant increase in prevalent syphilis among MSM after the introduction of combination antiretroviral therapy (cART), rising from 0.5% to 0.8% of the MSM population.¹⁵ Many studies posit that syphilis outbreaks among HIV positive MSM may be related to changes in sexual behaviour among this group. For example, effective cART may lead to reductions in safer sex practices among MSM who no longer fear AIDS-related complications such as opportunistic infections.^15–19

Shanghai has 17 million permanent residents and 5 million migrants. By the end of 2007, 3010 HIV/AIDS cases had been reported, of which 70% were migrants.²⁰ Shanghai is one of the largest metropolitan areas in China where the HIV/AIDS transmission route is largely attributed to homosexual contact. Some studies conducted in Shanghai found that substantial rates of unprotected sexual intercourse among MSM, and highlights the important role that social and financial contexts play in these behaviours. The rates of HIV-1 and syphilis infection were 4.4% and 10.3% of the MSM, respectively.²¹

Importantly, among many MSM, unprotected oral sex is considered a low-risk behaviour for HIV transmission, but is a route of transmission for syphilis and other sexually transmitted infections (STIs).^7,22 One recent study found that having more oral sex partners, receptive anal sex and unprotected receptive anal sex were all independently associated with greater odds of being infected with syphilis.²³

Few known studies in China have described prevalence and correlates of syphilis infection among HIV-positive MSM. Moreover, Shanghai had a great number of HIV-infected MSM with some typical social and behaviour characteristics, so we chose Shanghai as our survey area. The aims of this study are: (1) to better understand the prevalence of syphilis in a sample of HIV-positive MSM and (2) to examine the relationship between syphilis infection and demographic and behavioural factors. The findings of this paper will establish a basis for future interventions to prevent further transmission of STIs among HIV-positive MSM populations in China.

Methods

Participants

A cross-sectional survey was administered to HIV-positive MSM between June and December of 2010 in Shanghai, China. Inclusion criteria for the study were: (1) HIV-positive diagnosis confirmed by the local Shanghai CDC prior to the study; (2) infected with HIV via sex with men; (3) 18 years and older; and (4) reside in Shanghai during the study period. To facilitate our ability to reach the target populations, we collaborated with a non-governmental organization in Shanghai (Beautiful Life Health Promotion Center) with a history of outreach to HIV-positive MSM. Participants were recruited using snowballing methods. Initial participants were referred to the study by staff members at Beautiful Life Health Promotion Center. Beautiful Life Health Promotion Center services include providing HIV/AIDS education, counseling for cART, and mental health referrals. After completing the survey, participants were asked to refer other HIV-positive MSM in their peer networks to the study; participants were not compensated for providing referrals to the study. All referrals were screened via the inclusion criteria, specified above, and invited to participate in the study if they were eligible. Recruitment continued until 200 participants were enrolled in the study.

Procedures

Surveys were conducted in private rooms at our collaborating organization. Written informed consent was obtained from those who agreed to participate. Participants provide their written informed consent to participate in this study. The survey was administered face-to-face by trained staff in a confidential space. All participants received 30 Yuan (about $4) for participating in the study. This process was documented by the work staff of our research team. Study procedures and consent procedures were approved by the Anhui Medical University IRB.

Measures

We assessed socio-demographic characteristics including age, education, marital status, monthly income, and sexual orientation identity. STI- and HIV/AIDS-related knowledge were measured using a validated 18-item measure. We made the 18-item measures based on scale of HIV/AIDS related knowledge of China Ministry of Health. The eight questions of this scale only focus on general population, but in our research we want to explore the level of knowledge about HIV/AIDS in HIV-positive MSM. The questions we made in this scale included many domains which were closely related to HIV treatment and transmission and prevention of opportunistic infections in HIV-positive MSM; (sample item, “Does using a condom reduce the risk of HIV/ STI transmission?”; response options were “Yes,” “No,” and “I don’t know”). We assessed behavioural health information, including sexual behaviours with male partners (e.g. sexual position, the number of male anal sexual partners, HIV status of male sexual partners, etc.) and female sexual partners (e.g. the number of female sexual partners, HIV status of female sexual partners, the type of female sexual partners, etc.) in the past six months, condom use (e.g. condom use in the past six months and during the most recent sexual episode), alcohol consumption, alkyl nitrite use, and illicit drug use before having sex during the previous six months. We also collected the physical health information of the participants (the time of HIV diagnosis, receiving cART, reported CD4 lymphocyte counts at last test).

Laboratory testing

Blood samples were collected from all eligible participants for syphilis testing. Syphilis seropositivity was determined by rapid plasma reagin (RPR; Shanghai Kehua Biotechnology Co., Ltd Shanghai, China) and a Passive Particle Agglutination Test for detection of antibodies to Treponema pallidum (TPPA; Singapore MP Biomedical Asia Pacific Ltd Singapore, Singapore).

Statistical analysis

EpiData 3.0 (The EpiData Association, Odense, Denmark) software was used to input the survey data and Statistical Product and Service Solution (SPSS) 10.0 was used to analyse the data. We performed descriptive analyses to describe the demographic characteristics of participants and to examine the relationship between demographic characteristics and syphilis infection. Chi-square tests were conducted to examine the relationship between syphilis infection and behavioural characteristics during the six months prior to the participant’s interview. We conducted multivariable regressions to identify independent correlates of our primary dependent variable: syphilis infection. In order to identify variables for inclusion in the regression models, we used bivariate analyses to identify correlates of both dependent variables and included any co-factor that was associated with each dependent variable at P < 0.10. Regression models also included controls for sociodemographic variables expected to be associated with both dependent variables (Hosmer & Lemeshow, 2000).

Results

Participant characteristics and syphilis infection

A total of 200 HIV-infected MSM were enrolled in the study. Table 1 depicts the demographic characteristics of the sample population. The mean age was 36.3 (SD = 10.1) years and ages ranged from 21 to 68, with 45.0% of the sample being 26 to 35 years of age. Approximately one-third (30.0%) of the respondents reported being currently married to a woman. Participants currently living with a male partner and living with a female partner accounted for 17.0% and 9.0% of the total sample population, respectively. The majority (54.5%) had a Shanghai residence card. Over half of participants (55.0%) had at least a college education. Among all participants, 69.0% identified themselves as homosexual, 23.5% identified themselves as bisexual, and 7.5% identified themselves as heterosexual or unsure. Of the 200 participants who provided blood samples for this study, 33 (16.5%) tested positive for syphilis. Among participants living with male partners and female partners, approximately one-fifth (20.6%) and one-third (33.3%), respectively, tested positive for syphilis. No statistically significant differences in syphilis seroprevalence were observed among participants with respect to demographic characteristics.

Table 1.

Sociodemographic characteristics and syphilis infection of HIV-positive MSM sample (n = 200).

Variables	n (%)	Syphilis infection	χ ²	P value
Variables	n (%)	n (%)	χ ²	P value
Age group (years)			1.927	0.588
18-25	19 (9.5)	2 (6.1)
26-35	90 (45.0)	17 (51.5)
36-45	45 (22.5)	5 (15.2)
≥46	46 (23.0)	9 (27.2)
Marital status			0.398	0.881
Single	120 (60.0)	19 (57.6)
Currently married	60 (10.0)	10 (30.3)
Divorced/widowed	20 (30.0)	4 (12.1)
Living with a male partner			0.497	0.481
Yes	34 (17.0)	7 (21.2)
No	166 (83.0)	26 (78.8)
Living with a female partner			2.836	0.092
Yes	18 (9.0)	6 (18.2)
No	182 (91.0)	27 (81.8)
Having a Shanghai residence card			0.577	0.448
Yes	109 (54.5)	16 (48.5)
No	91 (45.5)	17 (51.5)
Education level			1.204	0.548
Junior high school or less	31 (15.5)	7 (21.2)
High school or vocational school	59 (29.5)	8 (24.2)
College or higher	110 (55.0)	18 (54.6)
Sexual orientation			0.093	1.000
Homosexual	138 (69.0)	23 (69.7)
Bisexual	47 (23.5)	8 (24.2)
Heterosexual/undecided	15 (7.5)	2 (6.1)

Table 2.

Relationship between syphilis infection and sexual behaviours during the past six months among HIV-positive MSM participants (n = 200).

Variables	n (%)	Syphilis infection	χ ²	P value
Variables	n (%)	n (%)	χ ²	P value
The most frequent venue for seeking male sexual partners			0.79	0.38
Internet	57 (28.5)	12 (36.4)
Gay venues^a	73 (36.5)	11 (33.3)
No sexual behaviours with men	70 (35.0)	10 (30.3)
Sex with male partners			0.86	0.84
Anal sex only	10 (5.0)	1 (3.0)
Oral sex only	15 (7.5)	2 (6.1)
Both anal and oral sex	105 (52.5)	20 (60.6)
None	70 (35.0)	10 (30.3)
Anal sex positioning			5.73	0.02
Insertive only	26 (13.0)	2 (9.5)
Both insertive and receptive	70 (35.0)	12 (57.1)
Receptive only	19 (9.5)	7 (33.4)
Number of anal sex partners			2.29	0.32
1	42 (21.0)	5 (23.8)
2	28 (14.0)	5 (23.8)
≥3	45 (22.5)	11 (52.4)
Frequency of anal sex per week			3.02	0.17
<1 time	90 (45.0)	14 (66.7)
1 ∼ 2 time	20 (10.0)	5 (23.8)
≥3 time	5 (2.5)	2 (9.5)
Had regular male sexual partner			0.73	0.39
Yes	61 (30.5)	8 (24.2)
No	139 (69.5)	25 (75.8)
Had casual male sexual partner			1.48	0.23
Yes	61 (30.5)	13 (39.4)
No	139 (69.5)	20 (60.6)
Had commercial male sexual partner			0.00	1.00
Yes	9 (4.5)	2 (6.1)
No	191 (95.5)	31 (93.9)
Inconsistent condom use during anal sex			2.00	0.16
Yes	32 (16.0)	8 (24.2)
No	168 (84.0)	25 (75.8)
Condom use in the last anal sex			0.00	1.00
Yes	107 (53.5)	19 (90.5)
No	8 (4.0)	2 (9.5)
Frequency of oral sex weekly			3.93	0.12
<1 time	98 (49.0)	15 (68.2)
1-2 times	17 (8.5)	5 (22.7)
≥3 times	5 (2.5)	2 (9.1)
Had vaginal sex with women			0.28	0.59
Yes	27 (13.5)	3 (9.1)
No	173 (86.5)	30 (90.9)
Inconsistent condom use during in vaginal sex			0.16	0.69
Yes	5 (2.5)	0 (0.0)
No	195 (97.5)	33 (100)
HIV status of sexual partners			9.88	0.01
HIV-positive	46 (23.0)	8 (24.2)
HIV-negative	18 (9.0)	8 (24.2)
Unknown	136 (68.0)	17 (51.6)
Alcohol use before sex			0.05	0.82
Yes	33 (16.5)	5 (15.2)
No	167 (83.5)	28 (84.8)
Alkyl nitrite abuse before sex			2.96	0.09
Yes	34 (17.0)	9 (27.3)
No	166 (83.0)	24 (72.7)
Illicit drug use before sex			0.68	0.41
Yes	5 (2.5)	2 (6.1)
No	195 (97.5)	31 (93.9)
Duration of HIV infection (years diagnosed)			0.32	0.85
<0.5	37 (18.5)	5 (15.2)
0.5-1	31 (15.5)	5 (15.2)
>1	132 (66.0)	23 (69.9)
CD₄ count (cells/mm³)			4.57	0.03
<500	175 (87.5)	26 (81.2)
≥500	15 (12.5)	6 (18.8)
Receiving antiretroviral therapy			3.24	0.07
Yes	144 (72.0)	28 (84.9)
No	56 (28.0)	5 (15.1)

Gay venues defined as gay bar, entertainment venues, bathhouse.

Relationship between syphilis infection and behaviour characteristics

Over half (57.5%) of participants in this sample reported having had anal sex with male partners and 16% of participants reported not using condoms consistently with male partners during the six months prior to the survey. Sixty percent of participants in the sample reported having had oral sex with male partners, and 47.0% reported any unprotected oral sex in the previous six months. Substance use measures included three categories: any alcohol consumption, any alkyl nitrite use, and any other illicit drug use. Prevalences of alcohol consumption, alkyl nitrite use, and illicit drug use before sex in the prior six months were 16.5%, 17.0%, and 2.5%, respectively.

Table 2 shows the relationship between syphilis infection and behaviour characteristics among participants who were syphilis/HIV co-infected; 63.6% reported having anal sex with male partners and 24.2% of participants reported unprotected anal sex during the previous six months. Approximately, two-thirds (66.7%) of co-infected participants reported having oral sex with male partners and 51.5% reported unprotected oral sex during the previous six months. The prevalences of alcohol consumption, alkyl nitrite use, and illicit drug use before sex among participants with co-occurring syphilis infection were 15.2%, 27.2%, and 6.1%, respectively.

Among participants who reported engaging in receptive anal sex with male partners in the previous six months, the prevalence of syphilis infection was 36.8%. Participants who reported having HIV-negative male sexual partners were more likely to be syphilis infected than those whose male sexual partners' HIV statuses were HIV-positive or unknown (44.4% vs.17.4% and 12.5%, χ²= 9.88, P = 0.01). In addition, respondents whose CD4 lymphocyte counts were 500 cells/mm³ or higher were more likely to be syphilis seropositive (40.0% vs.14.9%, χ² = 4.57, P = 0.03). Individuals who reported that the Internet was their most frequent place for finding male sexual partners had a syphilis prevalence of 21.1%, whereas those who reported gay gathering sites (e.g. entertainment venues, bathhouses) as their most frequent place for finding male sexual partners had a syphilis prevalence of 15.1%. The frequency of sex and the number of sexual partners were not related to syphilis status.

Logistic regression analysis of factors associated with syphilis infection

Multivariable logistic regression models examining correlates of syphilis infection are reported in Table 3. Significant correlates of syphilis infection included receptive anal sex with male partners in the past six months (AOR = 12.61, 90% CI = 2.38–66.89), illicit drug use in the past six months (AOR = 11.47, 90% CI = 2.47–53.44), and use of antiretroviral medication (AOR = 4.48, 90% CI = 1.43–14.05).

Table 3.

Multivariable logistic regressions: correlates of syphilis infection in HIV-positive MSM in China (n = 200).

Variables	Syphilis infection
Variables	Univariate regression OR (95% CI)	Multivariate regression OR (90% CI)
Age group (years)
18-25	Ref
26-35	1.979 (0.417–9.395)
36-45	1.062 (0.187–6.025)
≥46	2.068 (0.403–10.619)
Marital status
Single	Ref
Currently married	1.063 (0.460–2.456)
Divorced/widowed	1.329 (0.400–4.413)
Living with a male partner
No	Ref
Yes	1.396 (0.550–3.541)
Sexual orientation
Heterosexual/undecided	Ref
Homosexual	1.300 (0.275–6.153)
Bisexual	1.333 (0.251–7.096)
Sex with male partners
Anal sex only	Ref
Oral sex only	1.385 (0.108–17.670)
Both anal and oral sex	2.118 (0.254–17.689)
None	1.500 (0.171–13.160)
Anal sex positioning
Insertive only	Ref	Ref
Both insertive and receptive	2.483 (0.516–11.942)	3.781 (0.856–16.712)
Receptive only	7.000 (1.257–38.993)	12.608 (2.377–66.888)
Had regular male sexual partner
No	Ref
Yes	0.688 (0.291–1.627)
Inconsistent condom use during anal sex
No	Ref
Yes	0.524 (0.212–1.298)
Any illicit drug use in the past six months
No	Ref	Ref
Yes	4.469 (1.132–17.638)	11.486 (2.469–53.438)
Duration of HIV infection (years diagnosed)
<0.5	Ref
0.5-1	1.231 (0.321–4.716)
>1	1.350 (0.475–3.837)
CD₄ count (cells/mm³)
<500	Ref
≥500	3.821 (1.254–11.637)
Receiving antiretroviral therapy
No	Ref	Ref
Yes	2.462 (0.899–6.739)	3.848 (1.492–9.925)

Discussion

This study specifically examines HIV-infected MSM in China who are aware of their HIV infection. Our study showed a higher prevalence of syphilis (16.5%) among HIV-infected MSM compared with the general population of MSM in China (11.8%) and in Shanghai (11.7%).²⁴ Findings reported here are consistent with previous studies of syphilis prevalence in MSM. A survey of 477 MSM in Shanghai found a syphilis seroprevalence of 13.5%.²⁵ Another study of 2087 HIV patients in Shandong found a seroprevalence of syphilis of 19.6%.²⁶ In our study, the high prevalence (16.5%) of syphilis among MSM may indicate a high prevalence of unprotected sexual behaviours and suggests a potential risk of rapid HIV spread among MSM, although syphilis is more infectious than HIV. During the past six months, 57.7% reported having anal sex with male partners and 16% of participants reported not using condoms consistently with male partners. Previous studies in China had reported higher prevalence of unprotected anal sex in MSM. One study conducted in Chongqing included 1166 MSM, 14.8% of the participants had syphilis infection; furthermore, 35.1% reported unprotected anal sex in the past six months.²⁷

Among some MSM, unprotected oral sex is considered a safer sexual practice thus making oral sex a risk factor for transmission and acquisition of syphilis. Of note, 60.0% of participants in our study reported having oral sex with male partners with 47.0% reporting unprotected oral sex in the previous six months. Among the HIV/syphilis co-infected participants in our study, two-thirds reported having oral sex with male partners and half engaged in unprotected oral sex. A review of 65 articles found that the proportion of syphilis transmission attributable to oral sex is estimated to be between 20% and 46% in the USA and Europe.²⁸ Consequently, “positive prevention” efforts for HIV-infected MSM in China should caution against the STI risks associated with unprotected oral sex.

One interesting finding from our research was the relationship between of anal sex positioning and syphilis infection among HIV-positive MSM. We observed that participants had a more than 12-fold greater adjusted odds of testing positive for syphilis if they reported receptive anal sex versus insertive anal sex in the previous six months. It is possible that these men might perceive low added risk for engaging in unprotected receptive anal sex because they are already HIV infected. Our study design was cross-sectional, which limited our ability to define the relationship between engaging in receptive anal sex and syphilis infection. Receptive anal intercourse with male sexual partner has been repeatedly reported as a risk factor for HIV infection since early in the AIDS epidemic.²⁹ Our study included more participants who engaged in receptive anal sex than men who engaged in insertive anal sex. However, efforts also are needed to educate HIV-positive MSM of the potential for syphilis infection and other STIs due to unprotected sex, and of the adverse health consequences of co-infection of HIV and other STIs.

The majority of HIV-positive MSM diagnosed with syphilis in our study was already aware of their HIV-positive status and had been on cART for several years.³⁰ Interestingly, our study found that receiving cART was a risk factor for syphilis infection. On the one hand, in our research, the time sequence of HIV and syphilis diagnosis was unclear. However, the interaction between HIV and syphilis is complex. In addition, syphilis infection may increase the immune activation of host cells and the secretion of cytokines, and thus enhance HIV replication as well as decreases in CD4 cell counts.³¹ According to the national policy of China, patients receive cART only if their CD4 counts fall to below 250. But we cannot define whether in our study the reason for the fall in CD4 cell counts was syphilis infection. On the other hand, cART has significantly reduced AIDS-related mortality and is responsible for improved physical well-being, which may allow higher rates of sexual activity. These data are consistent with a study in Tel Aviv, Israel which indicated that HIV and syphilis co-infection was found to be more common in HIV-positive patients receiving cART.³² Together, these findings suggest that some HIV-positive patients may feel overly optimistic about their HIV disease being well-controlled, such that they perceive themselves as having low risk for additional STIs and subsequently engage in unsafe sexual behaviours.³³ Other international epidemiological studies highlight that the increased survival of high-risk HIV-infected MSM could lead to population level behaviour changes without necessarily changing the behaviour of specific individuals.^26,3,34 However, although some MSM are reporting high rates of unprotected sex, many others are adopting HIV risk reduction strategies, such as “sero-sorting” which refers to choosing partners with the same HIV status. Although sero-sorting prevents HIV transmission from an HIV-positive to an HIV-negative partner, the risk of syphilis and other STI transmission still remains.^30,32 It is also important to note that one of the most significant consequences of syphilis co-infection among HIV-positive MSM is its impact on the natural history of HIV infection and the increased risk of transmission of HIV. Thus, there is a need for a continued emphasis on syphilis prevention, as well as early diagnosis and treatment of syphilis in HIV-infected MSM in China.

In addition, consistent with other studies of risk behaviours related to syphilis infection among HIV-positive MSM,^26,32 our multivariate analysis found that illicit drug use was independently associated with syphilis infection among HIV-positive MSM. This may indicate that the use of illicit drugs is associated with unprotected sex, as some particular drugs are primarily used to enhance sexual pleasure and can also significantly impair judgment and/or reduce the ability to negotiate condom use through direct effects on mental function.^35,36

There are limitations to our study. The cross-sectional nature of the study prevents ascertainment of causal associations between related behaviours and syphilis infection. Longitudinal studies are needed to determine more causative relationships. Our relatively small sample size may limit the ability to recognize statistically significant behavioural associations associated with HIV/syphilis co-infection. Due to the hard-to-reach nature of the population of HIV-positive MSM, we used convenience sampling based on a snowball recruitment, which limits the generalizability of our findings. Additionally, we only interviewed MSM in Shanghai and, therefore, the sample might not be generalizable to HIV-infected MSM in other parts of China. In addition, self-reported data are subject to response bias. Participants were asked about sexual and drug use behaviours in the past six months, so recall bias may also be observed in our study. Finally, due to the scale of knowledge level in HIV-positive MSM which included three different domains, the validity and reliability of this scale might not be not high.

Data presented in this paper show a great deal of overlap among HIV and syphilis among MSM in China. High prevalence of syphilis in this population is associated with ongoing sexual risk behaviour which might be due in part to the success of cART which minimizes risk of opportunistic infections and reduces perceptions of illness severity and susceptibility. The tendency for people to increase risk behaviours when they perceive they are protected against harm (e.g. due to biomedical treatment) is referred to as risk compensation,³⁷ and this phenomenon might be contributing to increasing incidence of syphilis among HIV-positive MSM in China. Additional research is needed to examine understanding about sexual risk behaviours among HIV-positive MSM in China and the perceived susceptibility and consequences of further STIs. “Positive prevention” interventions are needed in China to continue educating HIV-positive individuals about behavioural and biological risks of STIs and strategies for reducing those risks, such as consistent condom use and partner sero-sorting practices. In addition, integrating HIV testing with testing and treatment for STIs – particularly in populations at high risk for co-infection such as MSM – may offer a useful strategy for education and behavioural risk reduction to avert new STIs in vulnerable populations in China. In China, we should set a STI sentinel surveillance system to evaluate the prevalence of HIV and other STI co-infection among MSM, changes in the HIV and STI epidemiology and increase in funding for prevention. This sentinel surveillance system also can provide behavioural characteristics and related information for analysis of trends in the HIV epidemic.

Author Contributions

HZ was responsible for designing this research, MW, YQ, and XS were responsible for conducting this research, ZD and DS were responsible for statistical analysis, HH was responsible for writing this paper, and HZ, NZ, and DO were responsible for revising this paper.

Footnotes

Acknowledgements

We thank the staff of Beautiful Life Health Promotion Center in Shanghai city for their help in recruiting participants, and we also the staff from the Center for Disease Control of Shanghai for their assistance in syphilis testing, as well as all participants in this study.

Conflict of interest

The authors declare no conflict of interest.

Funding

This study was supported by Natural Science Foundation of China (grant no. 30771850).

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