Original research article

International Journal of STD & AIDS

2014, Vol. 25(6) 410–419
! The Author(s) 2013
Prevalence of syphilis infection and Reprints and permissions:
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associations with sexual risk behaviours DOI: 10.1177/0956462413512804
std.sagepub.com
among HIV-positive men who have sex
with men in Shanghai, China

Huan He1, Min Wang1, Nickolas Zaller2, Jun Wang1,

Dandan Song1, Yuhuang Qu3, Xin Sui3, Zhengxin Dong1,
Don Operario4 and Hongbo Zhang1

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 anti-
retroviral 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 ¼ 12.61, 90% CI ¼ 2.38–66.89), illicit drug use in the past six months (AOR ¼ 11.47, 90%
CI ¼ 2.47–53.45), and use of antiretroviral medication (AOR ¼ 4.48, 90% CI ¼ 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, Treponema pallidum, men who have sex with men, MSM, China, risk
behaviour

Date received: 8 May 2013; accepted: 28 August 2013

Introduction HIV and syphilis share a common mode of transmis-

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 inci-
dence 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 preva-
lence 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
sion. Thus, the interaction between HIV and syphilis is
of importance in both sentinel surveillance and clinical
treatment of both infections. Among MSM popula-
tions, HIV infection has been shown to be strongly
associated with syphilis infection.7,8 A large body of
1
Department of Epidemiology and Health statistics, School of Public
Health, Anhui Medical University, Hefei, PR China
2
Department of Infectious Diseases, Alpert Medical School, Brown
University, Providence, RI, USA
3
Beautiful Life Health Promotion Center, Shanghai, PR China
4
Program in Public Health, Brown University, Providence, USA
Corresponding author:
Hongbo Zhang, School of Public Health, Anhui Medical University,
69 Meishan Road, Hefei 230032, Anhui Province, RI, PR China.
Email: zhb62@yahoo.com.cn

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He et al.
research conducted internationally among MSM sug-
gests 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 syph-
ilis.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 con-
ducted 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 posi-
tive MSM may be related to changes in sexual beha-
viour 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 metropol-
itan areas in China where the HIV/AIDS transmis-
sion 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 import-
ant 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 trans-
mission, 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 preva-
lence 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 find-
ings of this paper will establish a basis for future
interventions to prevent further transmission of
STIs among HIV-positive MSM populations
in China.
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411
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 collabo-
rated 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 complet-
ing the survey, participants were asked to refer other
HIV-positive MSM in their peer networks to the study;
participants were not compensated for providing refer-
rals to the study. All referrals were screened via the
inclusion criteria, specified above, and invited to par-
ticipate 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 colla-
borating 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 participat-
ing 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 includ-
ing 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
412
we made in this scale included many domains which
were closely related to HIV treatment and transmission
and prevention of opportunistic infections in HIV-posi-
tive 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 beha-
viours 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 partici-
pants 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 relation-
ship between syphilis infection and behavioural charac-
teristics during the six months prior to the participant’s
interview. We conducted multivariable regressions to
identify independent correlates of our primary depend-
ent variable: syphilis infection. In order to identify vari-
ables for inclusion in the regression models, we used
bivariate analyses to identify correlates of both depend-
ent variables and included any co-factor that was asso-
ciated with each dependent variable at P < 0.10.
Regression models also included controls for sociode-
mographic variables expected to be associated
with both dependent variables (Hosmer & Lemeshow,
2000).
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International Journal of STD & AIDS 25(6)
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 ¼ 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 edu-
cation. Among all participants, 69.0% identified them-
selves 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.
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 par-
ticipants 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 cate-
gories: any alcohol consumption, any alkyl nitrite use,
and any other illicit drug use. Prevalences of alcohol con-
sumption, 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 infec-
tion and behaviour characteristics among participants
who were syphilis/HIV co-infected; 63.6% reported
having anal sex with male partners and 24.2% of partici-
pants 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 alco-
hol 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.
He et al. 413

Table 1. Sociodemographic characteristics and syphilis infection of HIV-positive MSM sample (n ¼ 200).

Syphilis infection

Variables n (%) n (%) 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)

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%, 2 ¼ 9.88, P ¼ 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%, 2 ¼ 4.57, P ¼ 0.03).
Individuals who reported that the Internet was
their most frequent place for finding male sexual part-
ners had a syphilis prevalence of 21.1%, whereas
those who reported gay gathering sites (e.g. entertain-
ment 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 cor-
relates 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 ¼ 12.61, 90% CI ¼ 2.38–66.89), illicit
drug use in the past six months (AOR ¼ 11.47, 90%
CI ¼ 2.47–53.44), and use of antiretroviral medication
(AOR ¼ 4.48, 90% CI ¼ 1.43–14.05).
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 popula-
tion of MSM in China (11.8%) and in Shanghai
(11.7%).24 Findings reported here are consistent with

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414 International Journal of STD & AIDS 25(6)

Table 2. Relationship between syphilis infection and sexual behaviours during the past six months among HIV-positive MSM par-
ticipants (n ¼ 200).

Syphilis infection

Variables n (%) n (%) 2 P value

The most frequent venue for seeking male sexual partners 0.79 0.38
Internet 57 (28.5) 12 (36.4)
Gay venuesa 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)
(continued)

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He et al. 415

Table 2. Continued.

Syphilis infection

Variables n (%) n (%) 2 P value

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

Table 3. Multivariable logistic regressions: correlates of syphilis infection in HIV-positive MSM in China (n ¼ 200).

Syphilis infection

Univariate regression Multivariate regression

Variables OR (95% CI) 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)
(continued)

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416 International Journal of STD & AIDS 25(6)

Table 3. Continued.

Syphilis infection

Univariate regression Multivariate regression

Variables OR (95% CI) OR (90% CI)

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)

previous studies of syphilis prevalence in MSM. A
survey of 477 MSM in Shanghai found a syphilis sero-
prevalence 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 syph-
ilis is more infectious than HIV. During the past six
months, 57.7% reported having anal sex with male part-
ners and 16% of participants reported not using
condoms consistently with male partners. Previous stu-
dies in China had reported higher prevalence of unpro-
tected anal sex in MSM. One study conducted in
Chongqing included 1166 MSM, 14.8% of the partici-
pants had syphilis infection; furthermore, 35.1%
reported unprotected anal sex in the past six months.27
Among some MSM, unprotected oral sex is con-
sidered 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%

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He et al.
reporting unprotected oral sex in the previous six
months. Among the HIV/syphilis co-infected partici-
pants 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 propor-
tion 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 previ-
ous six months. It is possible that these men might per-
ceive 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 inter-
action between HIV and syphilis is complex. In add-
ition, 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
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417
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 inter-
national epidemiological studies highlight that the
increased survival of high-risk HIV-infected MSM
could lead to population level behaviour changes with-
out necessarily changing the behaviour of specific indi-
viduals.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 preven-
tion, 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 signifi-
cantly 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-sec-
tional 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 stat-
istically 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 add-
ition, self-reported data are subject to response bias.
Participants were asked about sexual and drug use beha-
viours in the past six months, so recall bias may also be
observed in our study. Finally, due to the scale of know-
ledge level in HIV-positive MSM which included three
different domains, the validity and reliability of this scale
might not be not high.
418
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 susceptibil-
ity. 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 stra-
tegies for reducing those risks, such as consistent
condom use and partner sero-sorting practices. In add-
ition, integrating HIV testing with testing and treat-
ment 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 sur-
veillance 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 ana-
lysis, HH was responsible for writing this paper, and HZ,
NZ, and DO were responsible for revising this paper.
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).
Downloaded from std.sagepub.com at UNIV OF WESTERN ONTARIO on June 11, 2015
International Journal of STD & AIDS 25(6)
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