Prevalence and the associated risk factors of HIV,STIs and HBV among men who have sex with men in Kunming,China

Abstract

To investigate the prevalence and the associated risk factors of human immunodeficiency virus (HIV), hepatitis B virus (HBV) and sexually transmitted infections (STIs) among men who have sex with men (MSM) in Kunming, 300 MSM were recruited through community-based organizations between September 2014 and January 2015. The prevalence of HIV, HBsAg, syphilis, Chlamydia trachomatis (CT) and Neisseria gonorrhoeae (NG) were 17.0%, 7.7%, 11.3%, 18.2% and 13.2%, respectively. In the three different anatomic sites (urethra, rectum and pharynx), the prevalence of rectal CT was the highest (15.5%), whereas NG was most commonly found in the pharynx (8.1%). Low education level, homosexuality, inconsistent condom use and drug use in the previous six months were significantly associated with HIV infection, whereas the former three factors were also associated with HBV infection.Older people (aged ≥ 40 years) and those who lacked knowledge of STIs, and younger people (aged <30 years) as well as inconsistent condom users were more at risk of syphilis and CT infections, respectively. NG infection was only associated with reported dating venues. Our study revealed a heavy disease burden and multiple risk factors of HIV/STIs among MSM in Kunming. It is necessary to promote regular screening and proactive treatment of HIV/STIs among MSM.

Keywords

Men who have sex with men human immunodeficiency virus hepatitis B virus sexually transmitted infections prevalence risk factors

Introduction

In the recent years, a fast-spreading human immunodeficiency virus (HIV) epidemic among men who have sex with men (MSM) constitutes a new public health challenge in China. The annual rate of newly reported HIV cases attributed to man-to-man transmission in China has increased from 2.5% in 2006 to 25.8% in 2014.¹ According to the national sentinel surveillance data, the prevalence of HIV infection among MSM has increased from 0.9% in 2003 to 7.7% in 2014.¹ A meta-analysis found that the national HIV incidence among Chinese MSM was 5.0 per 100 person-years (95% CI: 4.1–5.8%).² These data suggest that MSM remain one of the most important target populations for HIV prevention in China.

Since the first HIV epidemic in China was identified among people who inject drugs in Yunnan in 1989, Yunnan has been one of the provinces hardest hit by HIV.³ By the end of 2014, the cumulative number of reported HIV/AIDS cases in Yunnan reached 104,627, and the number of people living with HIV/AIDS was 80,610; these two figures were the highest when compared with other provinces in China. After 2006, the main transmission route changed from intravenous injection to sexual contact. Yet, the HIV prevalence (9.42–11.78%) and incidence (6.01–8.38%) remained stubbornly high among the MSM population in 2008–2010.⁴

It is well known that the presence of sexually transmitted infections (STIs) can increase the efficiency of HIV transmission.⁵ A prospective cohort study among MSM in Kunming showed that the relative risk of HIV seroconversion was 17.7 times higher in syphilis-positive MSM.⁶ At the same time, diagnosis and treatment of STIs in MSM offer a unique opportunity to identify high-risk MSM for preventive services. Except for syphilis, the prevalence and the associated risk factors of other STIs (Chlamydia trachomatis [CT] and Neisseria gonorrhoeae [NG]) and hepatitis B among MSM in Yunnan had not been elucidated in the past.

Kunming is the capital city of Yunnan province, where both the estimated number of MSM and the reported number of HIV-positive MSM accounted for more than half of the MSM population and MSM living with HIV in the whole province. In the present study, we examined HIV, STIs and hepatitis B virus (HBV) prevalence among MSM in Kunming and further evaluated the associated risk factors. These findings would be valuable to better understand the HIV/STIs epidemic and optimize HIV/STIs healthcare services for MSM individuals in Yunnan.

Methods

Enrolment of the study participants

This survey had a cross-sectional design and utilized convenience sampling to recruit MSM between September 2014 and January 2015. Two community-based organizations referred MSM to Yunnan Center for Disease Control and Prevention and Kunming Center for Disease Control and Prevention to participate in the study. Eligibility criteria included age ≥18 years, staying in Kunming for at least three months and having had anal sex with men in the last six months. Based on an estimated syphilis prevalence of 7.5% among MSM in Kunming with two-sided confidence interval of 95% and tolerant errors of ±3%, the calculated sample size should be larger than 296. Finally, a total of 300 MSM were chosen. Each participant was provided with the transport subsidy of 50 RMB. Written consents were obtained from all participants, and the study was approved by Biomedical Ethics Review Committee of Yunnan Province (LUNPI201402).

Questionnaire and sampling

The face-to-face interviews were performed by the trained investigators. Using face-to-face interviews, the investigators could not only collect the relative information but also perform health education and STI diagnosis, which was beneficial for treatment and care. The survey questionnaire included demographics, HIV/STI knowledge, sexual behaviors, number of sexual partners, condom use, whether they used drugs and health-seeking behavior. The judging criteria of mastering STI-related knowledge were to correctly answer seven of the following questions: (1) How many kinds of sexually transmitted infections are there in China? What are they? (2) Do all diseases that occur in the genital area belong to sexually transmitted infections? (3) Can avoiding multiple sexual partners reduce the risk of transmission of sexually transmitted infections? (4) Can condom use reduce the risk of transmission of sexually transmitted infections? (5) Can early detection and treatment of syphilis prevent mother-to-child transmission of syphilis? (6) Will one person who has ever contracted sexually transmitted infections be infected again? (7) Do sexual partners of patients with sexually transmitted infections need to be treated? (8) Can sexually transmitted infections be transmitted through eating? The condom use was measured by the participants’ self-reporting. “Consistent condom use” meant using a condom during every homosexual act in the past six months. From each participant, 5 ml of EDTA-anticoagulated peripheral blood, first pass urine (20 ml) and, rectal and pharyngeal swabs were collected.

Laboratory testing

HIV-1 infection status was screened using a rapid test (Determine, Alere Diagnostics, USA) and confirmed by Western blot assay (HIV BLOT 2.2, MP Diagnostics, Singapore). For syphilis testing, plasma samples were screened with an enzyme-linked immunosorbent assay (ELISA) kit (Hangzhou Aibo, China) and were confirmed with a Treponema pallidum particle agglutination assay (Serodia, Japan). Specimens positive for Treponema-specific antibody were further tested for non-specific antibody with a tolulized red unheated serum test test (Xiamen Xinchuan, China). The samples positive for both Treponema-specific antibody and non-specific antibody were used to calculate the prevalence of syphilis. HBsAg, HBsAb, HbeAg, HBeAb and HBcAB were detected with ELISA assays (Shanghai Kehua, China). For CT and NG testing by polymerase chain reaction, urine, rectal and pharyngeal swabs were tested with a COBAS 4800 CT/NG Test kit (Roche Molecular Systems Inc.)

Statistical analysis

Statistical analyses were conducted using the SPSS 19.0 statistical analysis software package (SPSS Inc., Chicago, IL). Categorical variables were compared using χ² tests. Risk factors associated with HIV, HBV, syphilis, CT and NG infections were analyzed with logistic regression. Variables in the multivariate logistic analysis were selected and entered into the model if they were marginally significant with P < 0.10 in univariate logistic analysis. All tests were two-tailed, and a P-value < 0.05 was considered statistically significant.

Results

Demographic characteristics of study participants

A total of 300 MSM were recruited in this study. The participants’ mean age was 31.3 ± 8.9 years (range: 18–74 years). The first homosexual encounter ranged from 12 to 48 years old with the mean age of 22.1 years old. Of all participants, 81.3% were native residents in Yunnan. Among these MSM, 15.3% were married to a female partner, of whom 50.0% were aged ≥40 years, 41.3% aged 30 to 39 years, and only 8.7% were aged <30 years. The demographic characteristics are shown in Table 1.

Table 1.

Demographic characteristics of study participants.

Demographic characteristics	Number (constituent ratio, %)
Age (years)
18–29	164 (54.6)
30–39	80 (26.7)
≥40	56 (18.7)
Place of origin
Yunnan	244 (81.3)
Other provinces	56 (18.6)
Education level
Junior middle school and below	86 (28.7)
Senior middle school/ technical secondary school	99 (33)
College and above	115 (38.3)
Occupation
Students	26 (8.7)
Enterprise/institute staff	37 (12.3)
Service workers	75 (25)
Unemployed	44 (14.7)
Others	118 (39.3)
Marital status
Unmarried	234 (78.0)
Married	46 (15.3)
Cohabitation	1 (0.3)
Divorced/widowed	19 (6.3)
Sexual orientation
Homosexual	213 (71.0)
Heterosexual	74 (24.7)
Others	13 (4.3)
Age of first homosexual encounter (years)
<20	159 (53.0)
≥20	141 (47)
Preferred dating place/manner
Internet	199 (66.3)
Bathroom	31 (10.3)
Others (bars, clubs, tearooms, parks and so on)	70 (23.3)

Sexual behaviors and condom use

In the previous six months, all participants had anal sex with men, while 14.7% of the participants also had sex with women (Table 2); 82.3% had used condoms in the last anal sex with a male partner – just over half (57.8%) admitted consistent condom use in the last six months, and 59.1% said they had used condoms with a female partner in the last sexual encounter, which was statistically lower than that with a male partner (χ²= 12.655, P = 0.01) where the proportion of consistent condom use in the last six months was 36.4%. Further, the homosexual behaviors were rather “fluid” with a mixture of fixed, temporary and commercial male sexual partners (Table 2).

Table 2.

Condom use for different sexual behaviors among the participants.

Sexual behaviors	Proportion (%)	Proportion who used a condom during last sex (%)	Proportion of consistent condom use in the last six months (%)
Having had homosexual sexual contact in the last six months	100.0 (300/300)	82.3 (247/300)	57.8 (174/300)
Regular male partner	65.0 (195/300)	73.8 (144/195)	54.9 (107/195)
Casual male partner	77.0 (231/300)	88.3 (204/231)	59.7 (138/231)
Commercial male partner	6.3 (19/300)	68.4 (13/19)	68.4 (13/19)
Having had heterosexual sexual contact in the last six months	14.7 (44/300)	59.1 (26/44)	36.4 (16/44)

In this study, only 281 participants responded to the question of whether they had oral sex in the previous three months, of whom 59.4% reported that they had oral sex; the great majority (97%) practiced oral-penile sex.

The prevalence of HIV, HBV and STIs

Serological tests showed that the prevalence of HIV, syphilis and HBsAg among the participants was 17.0% (51/300), 11.3% (34/300) and 7.7% (23/300) (Table 3). Of the 300 participants, 296 obtained the valid CT/NG results from the three types of specimens (Table 3). Overall, the prevalence of CT and NG was 18.2% (54/296) and 13.2% (39/296) among the participants, respectively. The prevalence of urethral, rectal, and pharyngeal CT was 3.7% (11/296), 15.5% (46/296) and 2.4% (7/296), respectively. The prevalence of CT at these three sites showed statistical difference (χ²= 46.508, P < 0.01) with the prevalence of rectal site being the highest. The prevalence of urethral, rectal and pharyngeal NG was 1.4% (4/296), 6.8% (20/296) and 8.1% (24/296), respectively. They were statistically different (χ²= 14.800, P = 0.01) with pharyngeal NG having the highest prevalence. HIV co-infections with STIs and/or HBV were also found in 11.0% of the participants.

Table 3.

The prevalence of HIV, HBV and STIs among the participants.

Test items	Number of the samples successfully tested	Number of the samples with a positive result	Prevalence (%)	χ²	P
HIV	300	51	17.0
Syphilis	300	34	11.3
CT	296	54	18.2
Urethral CT	296	11	3.7	46.508	<0.01
Rectal CT	296	46	15.5
Pharyngeal CT	296	7	2.4
NG	296	39	13.2
Urethral NG	296	4	1.4	14.800	0.01
Rectal NG	296	20	6.8
Pharyngeal NG	296	24	8.1
HBV	300	23	7.7
HBsAg	300	23	7.7
HBsAb	300	170	56.7
HBeAg	300	3	1
HBeAb	300	27	9
HBcAb	300	31	10.3

CT: Chlamydia trachomatis; HBV: hepatitis B virus; NG: Neisseria gonorrhoeae.

Risk factors associated with HIV/STI infections

Risk factors associated with HIV, HBV, syphilis, CT and NG infections were analyzed with logistic regression (Table 4). The multivariate analyses revealed that junior middle school education level or below, homosexual orientation, drug use and inconsistent condom use during homosexual anal sex in the previous six months were significantly associated with HIV infection; junior middle school education level or below, homosexual orientation and inconsistent condom use during homosexual anal sex in the previous six months were significantly associated with HBV infection; aged 40 years and above, and lack of STI knowledge were significantly associated with syphilis infection; aged below 30 years and inconsistent condom use during homosexual anal sex in the previous six months were significantly associated with CT infection; the preferred dating venues such as bars, clubs, tearooms and parks were significantly associated with NG infection.

Table 4.

Factors associated with HIV, HBV, syphilis, CT and NG infection among MSM in Kunming, China.

Factors	Univariate analysis		Multivariate analysis
Factors	OR (95% CI)	p	OR (95% CI)	p
HIV
Age (years)
≥40	1		1
30–39	1.87 (0.75–4.64)	0.95	3.03 (1.03–8.88)	0.04
<30	1.03 (0.43–2.44)	0.18	1.56 (0.57–4.27)	0.39
Education level
Junior middle school above	1		1
Junior middle school	7.56(2.74–20.8)	<0.01	3.32 (1.48–7.46)	<0.01
Illiteracy and primary school	2.52(1.21–5.02)	0.01	8.66 (2.73–27.46)	<0.01
Sexual orientation
Bisexual	1		1
Homosexual	2.28 (0.98–5.34)	0.06	4 .57 (1.60–13.07)	0.01
Unknown	3.19 (0.70–14.6)	0.14	3.83 (0.59–25.09)	0.16
Drug use
No	1		1
Yes	39.46 (4.74–328.60)	<0.01	45.82 (4.91–427.64)	0.001
Condom use during homosexual anal sex in the last six months
Consistent	1		1
Inconsistent	3.41 (1.81–6.45)	<0.01	2.72 (1.34–5.54)	0.01
HBV
Education level
Junior middle school above	1		1
Junior middle school	2.46 (0.95–6.40)	0.07	2.69 (1.00–7.25)	0.05
Illiteracy and primary school	5.27 (1.49–18.7)	0.01	1.59 (1.19–17.65)	0.03
Sexual orientation
Bisexual	1		1
Homosexual	7.98 (1.06–60.44)	0.04	7.98 (1.06–60.44)	0.04
Unknown	6.64 (0.39–113.97)	0.19	6.64 (0.39–113.97)	0.19
Condom use during homosexual anal sex in the last six months
Consistent	1		1
Inconsistent	3.47 (1.38–8.71)	0.01	3.23 (1.25–8.35)	0.02
Syphilis
Age (years)
<30	1		1
30–39	1.47 (0.60–3.61)	0.40	1.56 (0.63–3.84)	0.34
≥40	3.17 (1.35–7.44)	0.01	3.50 (1.46–8.34)	0.01
Whether knowledgeable of STIs
Yes	1		1
No	1.91 (0.90–4.09)	0.09	2.47 (1.11–5.51)	0.03
CT
Age (years)
≥40	1		1
30–39	3.69 (1.17–11.6)	0.03	4.01 (1.26–12.75)	0.02
<30	3.05 (1.03–9.08)	0.05	3.35 (1.11–10.01)	0.03
Condom use during homosexual anal sex in the last six months
Consistent	1		1
Inconsistent	2.04 (1.12–3.70)	0.02	2.17 (1.19–3.98)	0.01
NG
Age (years)
≥40	1		1
30–39	2.24 (0.68–7.36)	0.18	3.07 (0.90–10.49)	0.07
<30	2.05 (0.68–6.23)	0.20	3.01 (0.94–9.71)	0.07
Condom use during homosexual anal sex in the last six months
Consistent	1		1
Inconsistent	1.12 (0.57–2.21)	0.75	1.09 (0.10–1.07)	0.82
Preferred dating place/manner
Internet	1		1
Bathroom	1.30 (0.41–4.08)	0.66	1.73 (0.52–5.73)	0.37
Others (bars, clubs, tearooms, parks and so on)	2.19 (1.04–4.59)	0.04	2.72 (1.26–5.91)	0.01

CT: Chlamydia trachomatis; HBV: hepatitis B virus; NG: Neisseria gonorrhoeae.

Discussion

The overall STI prevalence for the participants in our study was 33.7%, which means one-third of the participants were infected with at least one kind of STI. Of the participants, the younger MSM (age <30 years) accounted for over half of the sample (54.6%), and the age of the first homosexual encounter was very young. A recent multicenter cross-sectional survey showed that the median age at first anal intercourse steadily decreased from 33 years of age among MSM born from 1940 to 1959 to 18 years of age among MSM born from 1990 to 1996.⁷ All of these suggested that sexual health education should be extended to the teenagers in- and out-of-schools. In China, the estimated prevalence of bisexual behavior among MSM is 31.2%,⁸ and 17.0% are married to a woman.⁹ In this study, we found 15.3% of the participants were married and 14.7% had heterosexual behaviors in the last six months. The bisexual behaviour mediated HIV/STI transmitting across sub-populations, which was supported by our previous molecular epidemiological study.¹⁰

This study showed that the internet/dating apps had become the most preferred way (66.3%) of making contacts in MSM. However, we did not find that preferentially using internet/dating apps to meet partners was an independent risk factor for HIV/STI infection in MSM, which conflicted with some earlier studies.¹¹ Actually, we found the proportion of consistent condom use in the last six months was higher in MSM preferentially using internet/dating apps to meet partners (62.3% vs. 49.5% in MSM dating through other means, χ²= 4.511, P = 0.036). Perhaps, it resulted from sexual health education delivered via social and sexual networking applications. In the last two years, we worked with four MSM working groups to increase testing and deliver sexual health information through internet/dating apps. Because of stigma and social discrimination, most MSM are unwilling to disclose their sexual identity, which hampers access to HIV testing and health information. However, the internet/mobile apps-based health information could provide a suitable platform for health promotion while preserving confidentiality. Thus, mobile technology presents an opportunity for innovative interventions for HIV prevention.

A previous meta-analysis showed that MSM in Southwest China had the highest HIV prevalence in comparison with other regions.¹² In Chengdu (the capital city of Sichuang Province), the overall HIV prevalence among MSM was 15.5% between 2009 and 2014.¹³ The reported HIV prevalence among MSM in Chongqing, the biggest city in Southwest China, ranged from 10.9% to 16.8%.¹⁴ According to the MSM sentinel surveillance, the prevalence of HIV-1 among MSM in Kunming was 10.0% in 2010.¹⁵ In this study, a highest-ever reported HIV prevalence of 17.0% was found among MSM in Kunming with 33 newly-diagnosed cases reflecting the huge challenge of controlling this epidemic for both policymakers and frontline professionals.

In this study, we found that low education level, homosexual orientation, drug use and inconsistent condom use during anal sex in the previous six months were independent risk factors for HIV infection in MSM. In the previous studies, low education level was often found to be associated with HIV infection among MSM in China.² Injection drug use (IDU) and recreational drug use (RDU) were not further distinguished in the questionnaire. According to the previous studies, IDU is rare among Chinese MSM;¹⁶ however, RDU is relative common.^17–19 RDU may increase risks for HIV/STI by disinhibiting cognitive function, impairing judgment such as safer sex practices and/or heightening sexual desire.^19,20 According to a cross-sectional study in six Chinese cities, men with RDU were more likely to report multiple sexual partners (OR = 1.69; 95% CI: 1.44–1.98) and unprotected sex (OR = 1.25; 95% CI: 1.05–1.49).¹⁷

Condoms are highly effective in HIV prevention; however, condom use by MSM is unsatisfactory. We found in our cohort that the proportion of consistent condom use in homosexual anal sex in the previous six months was low at 57.8%. Inconsistent condom use was demonstrated as a pivotal risk factor in a number of studies.² A recent survey in Yunnan indicated that the factors influencing condom use among MSM included cohabiting, low awareness of HIV/AIDS knowledge, being from other provinces, local residence for <1 year, low education level, receiving no intervention, frequent anal sex and receiving no HIV/AIDS detection.²¹ Based on mathematical modeling, even enhanced levels of HIV testing and linkage to care (TLC) and antiretroviral therapy (ART) among MSM will not interrupt epidemic expansion; however, TLC/ART plus condom use is expected to decrease the HIV epidemic,²² which suggests that condom use needs further promoting even under the circumstance of mass screening and early treatment among MSM.

There have been considerable studies on the risk factors for HIV acquisition in MSM in China; yet traditional behavioral intervention has not been effective.²³ In addition to the interventions aimed at the associated risk factors, interventions such as active care and early ART that targeted HIV-positive MSM should be actively promoted, which, in turn, could improve their quality of life and decrease further HIV transmission by lowering the community viral load²⁴; but first of all, we need to identify them. In this study, with the support from the CBO volunteers, the newly HIV-1 diagnosed MSM were referred for antiretroviral treatment. Oral antiretroviral drugs as prophylaxis could potentially prevent HIV infection among HIV-seronegative MSM and their partners.²⁵

In China, the overall prevalence of syphilis in MSM increased from 6.9% to 11.8% between 2003 and 2009.¹⁴ The syphilis prevalence in MSM was higher in some areas for example, 25.4% in Shenyang,²⁶ 20.34% in Jiangsu²⁷ and 19.8% in Beijing.²⁸ Here, we found that the syphilis prevalence among MSM in Kunming was 11.3%, which was obviously higher than that were reported in the previous study.⁶ Unexpectedly, the overall prevalence of CT and NG in the participants reached 18.2% and 13.2%, respectively. Furthermore, the prevalence of CT and NG showed differences in three different anatomic sites (urethra, rectum and pharynx), and the differences were in line with the results from a meta-analysis about CT/NG infection in MSM.²⁹ This suggested that unprotected anal and oral sex were more likely to be associated with the spread of CT and NG among MSM. In practice, clinicians should fully assess the risks of STIs by skilled inquiry and collect samples from different sites based on sexual activities. Sexually Transmitted Diseases Treatment Guidelines (Centers for Disease Control and Prevention, the United States, 2015) recommend that men who have had insertive intercourse should receive a test for urethral infection with CT and NG; men who have had receptive anal intercourse should receive a test for rectal infection with CT and NG; men who have acknowledged participation in receptive oral intercourse should receive a test for pharyngeal infection with NG, but not for pharyngeal infection with CT.

We found that younger age of below 30 years was a risk factor for both syphilis and CT. This suggested that young MSM may have more unsafe sexual behaviors and lacked awareness and knowledge of preventing STIs. Thus, it is necessary to strengthen the health education of STIs among MSM and particular efforts be made to reach and deliver services for young MSM. We also found that the prevalence of NG was higher among MSM dating at bars, clubs, tearooms and parks, which emphasises the role of casual sexual partners in the acquisition of NG infection. Thus, it is important to strengthen interventions in entertainment venues to reduce unsafe sexual behaviors. Given that these bacterial STIs are curable, regular testing and treatment can efficiently prevent and control their spread among MSM.

Hepatitis B does not belong to the classical STIs, but HBV can be transmitted through sexual contact. A national survey showed that the weighted prevalence of HBsAg for Chinese population aged 1–59 years was 7.2%.³⁰ In this study, the prevalence of HBsAg among MSM was 7.7%. We also found HBV infection among MSM shared risk factors with HIV infection. Nowadays, due to hepatitis B vaccination, the prevention of hepatitis B is highly efficient among the general population. To reduce HBV infection among MSM, free HBV vaccination should be considered as one part of MSM healthcare services. In this study, free HBV vaccination was provided to those whose HBV test results were negative.

In this study, because there were different sexual practices among MSM, the samples from different anatomic sites were collected for CT/NG testing, which was not reported in the previous studies in China, and we are the first to report the high prevalence of STIs in west China. However, there were a few limitations in our study. First, because MSM is a hidden population, selection bias cannot be completely avoided. Second, because some data were self-reported, reporting bias could be a threat to validity. Third, some key information was missing from the questionnaire, such as further information about drug use.

In conclusion, our study elucidated the high prevalence of HIV, HBV and STIs among MSM in Kunming. Behavioral interventions and health education for HIV and STIs should be enhanced continually. Meanwhile, health service providers should consider providing biological and medical measures to screen, treat and prevent infections.

Footnotes

Authors’ contribution

XZ, MJ and MC contributed equally to this article.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by World Health Organization (‘Implementing WHO recommendations for strengthening STI prevention and care services for men who have sex with men-development of service delivery model in Kunming’, CHN-13-HSI-000936).

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