Worsening Epidemic of HIV and Syphilis Among Men Who Have Sex With Men in Jiangsu Province, China

High HIV and syphilis incidence rates and prevalence among men who have sex with men in 2 cities of Jiangsu province indicate potential worsening of these epidemics in this population. Targeted intervention strategies are needed.

Abstract

Background. Epidemics of human immunodeficiency virus (HIV) and syphilis among men who have sex with men (MSM) are major public health concerns in most parts of China. A dearth of information regarding the current trend of HIV in this hard-to-reach population in several regions including Jiangsu, coupled with the reemergence of syphilis, calls for an effort to understand the dynamics of the dual epidemic in this province.

Methods. To estimate the occurrence and burden of these 2 sexually transmitted diseases and the distribution of their potential sociobehavioral correlates among MSM in Jiangsu, 2 cohort studies were conducted in Yangzhou and Changzhou cities.

Results. Among 839 participants, 48% were married, 51.7% had sex with women in the last 6 months, and 25.5% did not use condoms during their last anal intercourse. The observed incidence of HIV was 13.59 and 12.62 and that of syphilis was 7.33 and 13.25 per 100 person-years among the participants of Yangzhou and Changzhou, respectively. The baseline prevalence of HIV and syphilis was 16.0% and 29.9% in Yangzhou and 13.6% and 14.9% in Changzhou, respectively.

Conclusions. Considerably high incidence and prevalence of HIV and syphilis among participants and their potential bridging role in transmitting these infections to the general population in Yangzhou and Changzhou cities calls for urgent effective intervention strategies.

(See the Editorial Commentary by Mayer on pages 1760–2.)

The human immunodeficiency virus (HIV) epidemic has now concentrated among men who have sex with men (MSM) in China [1], and this expanding epidemic among MSM is currently China's biggest public health concern [2, 3]. Nationally, the proportion of sexually transmitted HIV cases increased from 33.1% in 2006 to 76.3% in 2011, and homosexual transmission played a significant role [4]. In 2009, about 8.6% of all and 29.4% of new HIV infections (12.2% in 2007) occurred through sexual acts between men in this country [5]. The prevalence of HIV among MSM also increased in Beijing (from 0.4% in 2004 to 6.3% in 2010) [6, 7], Shenzhen (from 0.9% in 2002 to 5.3% in 2008) [8, 9], and Chongqing (from 10.4% in 2006 to 16.7% in 2008) [10, 11]. Average HIV prevalence among urban MSM was 5% during a survey in 2008–2009 involving 61 cities [3].

The expanding epidemic of syphilis (prevalence in 2010 was 20.0 cases per 100 000) is another major concern in China [12] and threatens to exacerbate the HIV epidemic, as syphilis infection may facilitate HIV transmission [13]. Unprotected sex between MSM and otherwise low-risk women (wives/regular partners) and the HIV/syphilis epidemic among MSM pose a serious threat to the general population [14–16].

Evidence regarding the incidence and trend of HIV and syphilis among MSM was unavailable in Jiangsu province. In 2008, to understand the characteristics of these epidemics among MSM, a national comprehensive HIV prevention and care pilot program was conducted in 61 cities, including Yangzhou city in Jiangsu where the scenario was found to be one of the worst in China [3]. Two contemporary surveys also revealed HIV and syphilis burdens of 9.33% and 22.8%, respectively, among MSM in this city [3, 17]. Changzhou, another nearby city in the same province, had previously shown a worrisome HIV and syphilis epidemic situation. A prospective monitoring and evaluation of the current trends of HIV and syphilis epidemic among MSM in Jiangsu was thus called for.

MATERIALS AND METHODS

Study Design and Objectives

Two concurrent cohort studies were conducted in Yangzhou and Changzhou cities of Jiangsu between July 2009 and December 2010, to estimate the incidence and prevalence of HIV and syphilis among MSM and to evaluate their potential bridging role in transmission of HIV and other sexually transmitted infections (STIs) to other populations.

Study Participants

Cruising areas and service points (eg, STI clinics) for MSM were listed and mapped by local governmental and nongovernmental organizations in Changzhou and Yangzhou. Site-specific sampling periods were determined based on attendance and hours of operation. Men who attended the sites during the study period, had sex with men (oral and/or anal) within the past year, were aged 18 years or older, and provided written informed consent were recruited at the scheduled sites between July and October 2009. Individuals who had medical reasons or intoxication preventing them from active participation or who were currently or previously enrolled in any behavioral intervention trial in the past 3 months were excluded.

Structured Interview

Eligible participants were interviewed with a structured questionnaire to collect information on demographics, HIV-related knowledge, coverage of HIV prevention services, recent sexual behavior (including commercial sex with men and heterosexuality), and drug use.

Demographic information included age (<20, 20–29, 30–39, 40–49, and ≥50), marital status (never married to a woman, married to woman during survey, and divorced/widowed), education level (elementary school or lower, junior or senior high school, college or higher) and residency (“hukou”) status (official resident of Yangzhou and Changzhou cities/other cities in Jiangsu province/other province). Cruising areas/venues were categorized as pubs/discos/tearooms/clubs, spas/bathhouses/saunas/massage parlors, internet, parks/public restrooms/other public areas, and college campus/introduced by friends.

Recent sexual behavior was assessed by the number of male partners in the past 6 months and whether condoms were used or not during the last anal (with casual or regular partners) and vaginal intercourse.

Serological Measures

In each round of the study, HIV antibody positivity was screened by a rapid test (Acon Biotech) and confirmed by Western blot (HIVBLOT 2.2, Genelabs Diagnostics, Singapore), and HIV-negative specimens were further screened by RNA testing to reduce the potential for false negatives (due to window period). Participants positive for both enzyme-linked immunosorbent assay (Wantai Biopharmacy) and toluidine red unheated serum test (Wantai Biopharmacy; a qualitative and quantitative card test for the serologic detection of syphilis) were defined as syphilis positive.

Cohort Follow-up

After the baseline interview, all participants (except HIV-positive individuals, who were referred to HIV care programs) were encouraged to attend the follow-up surveys (after 6 and 12 months) and were reminded 2 weeks prior to the scheduled date. The retention rate was defined as participation in successive rounds compared with the initial round (excluding positives from denominator in each round).

HIV and syphilis incidence rates were estimated by using the number of seroconversions within each follow-up period as the numerator and the cohort's total person-years at risk (of respective disease, including those for subjects lost to follow-up in the next follow-up period) within each follow-up period as the denominator. For those who seroconverted, half of the follow-up duration (between 2 follow-ups) was used as their contribution to the total person-time at risk. Because knowing the exact date for HIV or syphilis seroconversion during the follow-up period was impossible, the middle point of the duration was used as a proxy for the date of seroconversions, to potentially reduce the overall misclassification of the contributed person-time.

Data Analysis

Data were double-entered using EpiData 3.0 [18] using logic checks. Descriptive analyses (including 95% confidence intervals [CI]) of demographics and sexual behavior were conducted and prevalence of both the diseases was determined. HIV and syphilis incidence rates were calculated by Poisson χ² method. SAS version 9.1 [19] was used for analyses.

Ethical Statement

The study process and content were approved by the Ethics Committee of Jiangsu Provincial Center for Disease Prevention and Control. Signed informed consent was obtained from each participant prior to the interviews and blood collection at each round. All electronic and printed documents were securely preserved with confidentiality.

RESULTS

Overall, 839 participants (Figure 1) completed the baseline survey (484 for Changzhou and 355 for Yangzhou). About 67.3% were 20–39 years old, 46.2% met their partners mainly at bathhouses (56.7% for Yangzhou and 38.3% for Changzhou), about half were married to woman (59.7% for Yangzhou and 38.3% for Changzhou), and less than one-third had attended college or higher (23.7% for Yangzhou and 29.8% for Changzhou) (Table 1).

Figure 1.

Study flowchart of the men who have sex with men (MSM), with focus on the human immunodeficiency virus (HIV) and syphilis incidence cohort (N = 839).

Table 1.

Baseline Distribution of Sociobehavioral Factors and Burden of HIV Among Participating Men Who Have Sex With Men in the Cohort (N = 839)

Variable	Yangzhou (n = 355)a			Changzhou (n = 484)a			Total (N = 839)
	Frequency	%	95% CI	No.	%	95% CI	Frequency	%
Age, y
<20	17	4.7	1.5–7.8	26	5.8	3.6–8.0	43	5.4
20–29	155	43.6	36.1–51.1	179	40.0	35.5–44.6	334	41.6
30–39	78	22.1	15.8–28.4	127	28.4	24.2–32.6	205	25.5
40–49	89	25.0	18.5–31.5	88	19.7	16.0–23.4	177	22.0
≥50	17	4.7	1.5–7.8	27	6.0	3.8–8.3	44	5.5
Education
Elementary or less	15	4.2	2.1–6.3	24	5.0	3.0–6.9	39	4.6
Junior/senior high school	246	69.3	64.5–74.1	307	63.4	59.1–67.7	553	65.9
College or higher	94	26.5	21.9–31.1	153	31.6	27.4–35.8	247	29.4
Marital status
Never married to a woman	167	47.0	41.8–52.2	248	51.2	46.8–55.7	415	49.5
Currently married to woman	164	46.2	41.0–51.4	206	42.6	38.1–47.0	370	44.1
Divorced/widowed	24	6.8	4.1–9.4	30	6.2	4.0–8.4	54	6.4
Venuesb
Pubs, discos, tearooms, clubs	74	21.0	16.7–25.2	149	30.9	26.8–35.0	223	26.6
Spas, bathhouses, saunas, massage parlors	199	56.4	51.2–61.6	180	37.3	33.0–41.7	379	45.2
Internet	60	17.0	13.0–20.9	89	18.5	15.0–22.0	149	17.8
Parks, public restrooms, other public areas	5	1.4	.2–2.6	7	1.4	.4–2.5	12	1.4
College campus, introduced by friends	10	2.8	1.1–4.6	31	6.4	4.2–8.6	41	4.9
Sexual relationship
Only with male	67	19.0	14.9–23.2	141	29.5	23.4–33.6	208	25.1
Mainly with male	64	18.2	14.1–22.2	136	28.4	24.4–32.5	200	24.1
Almost equally with male and female	103	29.3	24.5–34.0	130	27.2	23.2–31.2	233	28.1
Mainly with female	118	33.5	28.6–38.5	71	14.8	11.6–18.0	189	22.8
Had anal intercourse with men	266	74.9	70.4–79.5	311	64.3	60.0–68.5	577	68.8
Had sex with women	204	57.5	52.3–62.6	230	47.5	43.0–52.0	434	51.7
Unprotected anal intercourse with men	78	29.5	24.0–35.1	68	22.0	17.4–26.6	146	25.5
Unprotected vaginal intercourse	143	70.1	63.0–76.2	101	43.9	37.4–50.4	244	56.2
Paid money to female sex workers for sex	9	2.6	1.2–5.0	61	12.6	9.9–16.0	70	8.4
Engaged in sadomasochism	3	0.8	0–1.8	27	5.6	3.5–7.6	30	3.6
HIV positive	57c	16.1	12.5–20.4	66	13.6	10.8–17.1	123	15.0
Syphilis positive	106	29.9	25.2–35.0	72	14.9	11.9–18.4	178	21.2

Abbreviations: CI, confidence interval; HIV, human immunodeficiency virus; MSM, men who have sex with men.

^a Participants in each city.

^b Venues was defined as the place where MSM usually meet their casual sexual partners.

^c Including 3 RNA test–positive participants.

In the past 6 months, 68.8% were engaged in anal sex with men at least once; 25.5% of those who had anal sex did not use a condom during the last anal intercourse with men. Meanwhile, 51.7% of the participants also had sex with women in the past 6 months and more than half of them did not use a condom during the last vaginal intercourse.

At baseline, HIV and syphilis prevalence for participating MSM was 16.0% and 29.9%, respectively, in Yangzhou and 13.6% and 14.9%, respectively, in Changzhou (combined 15.0% and 21.2% for HIV and syphilis, respectively).

The retention rate at 6 months was 65.1% for Changzhou, and 60.7% for Yangzhou, and at 12 months was 36.0% for Changzhou and 16.4% for Yangzhou. Among participants of Changzhou, there were 66, 26, and 3 HIV-positive participants at baseline, 6 months, and 12 months respectively. Also, among participants of Yangzhou, there were 57 (including 3 RNA test–positive cases), 17, and 3 HIV-positive participants at baseline, 6 months, and 12 months, respectively (Figure 1).

Overall, the HIV incidence rate per 100 person-years was 12.6 (95% CI, 8.0–17.2) in Changzhou, 13.6 (95% CI, 7.6–19.6) in Yangzhou, and 13.0 (95% CI, 9.4–16.6) altogether. The overall syphilis incidence rate per 100 person-years was 13.2 (95% CI, 8.1–18.4) in Changzhou, 7.3 (95% CI, 2.4–12.4) in Yangzhou, and 11.1 (95% CI, 7.3–14.7) altogether (Table 2).

Table 2.

HIV and Syphilis Incidence Rates Among Men Who Have Sex With Men in Changzhou and Yangzhou, 2009–2010 (N = 839)

Disease	City	0–6 mo				6–12 mo
		Total PY	Person-time for Seroconverted Participants	No. of Seroconverted Participants	Incidence (per 100 PY)	Total Person-time	Person-time for Seroconverted Participants	No. of Seroconverted Participants	Incidence (per 100 PY)
HIV	Changzhou	188.1	10.9	26	14.7(9.0–20.3)	54.5	1.8	3	5.7 (0.2–12.1)
	Yangzhou	125.5	6.0	17	14.2 (7.5–21.0)	29.0	1.4	3	10.87 (0.1–22.9)
Syphilis	Changzhou	153.2	5.6	15	10.16 (5.0–15.3)	43.0	1.8	10	24.3 (9.3–9.5)
	Yangzhou	94.9	4.0	8	8.80 (2.7–14.9)	18.2	0.0	0	0.0
Disease	City	Overall
		PY /Disease/City		Incidence/100 PY/City		Total PY		Incidence for 2 Cities (per 100 PY)
HIV	Changzhou	229.9		12.6 (8.0–17.2)		377.0		13.0 (9.4–16.6)
	Yangzhou	147.1		13.6 (7.6–19.6)
Syphilis	Changzhou	188.7		13.3 (8.1–18.4)		297.8		11.1 (7.3–14.9)
	Yangzhou	109.1		7.3 (2.2–12.4)

Abbreviations: HIV, human immunodeficiency virus; PY, person-years.

DISCUSSION

This cohort study in Changzhou and Yangzhou cities of the Jiangsu province of China revealed alarmingly higher HIV and syphilis incidence rates and prevalence among the participating MSM compared with contemporary observations in China [20, 21], the United States [22, 23], Canada [24], Europe, and Australia [25].

High HIV incidence rates as observed among our participants probably indicated an increase in the occurrence of new HIV infections through male-to-male sexual contact in the study area. New HIV infections among MSM increased from 12.2% in 2007 to 32.5% in 2010 in China [2, 26] and are expected to be even higher in Jiangsu province, as sexual contact (including the considerable role of homosexuality) is the main transmission route (higher than the national proportion of 76% in 2009) in China [2].

Moreover, observed high syphilis incidence rates among the participants indicated a potential deterioration of the HIV scenario as syphilis infection is a known risk factor for HIV acquisition and shares similar transmission routes [27–29]. Syphilis infection might also have increased the immune activation of host cells and secretion of cytokines, resulting in enhanced HIV replication and shortening of the latency or incubation period for progression to AIDS [29].

The fact that incidence rates for HIV and syphilis were much higher during the initial 6 months than in the later follow-up period may be due to decreased STIs owing to treatment, reduction in risk behaviors over time under the influence of consistent voluntary counseling and testing, or losses to follow-up. Some of the early infections could also be eclipse infections (<11 days, antibody negative, RNA negative), although the impact was expected to be minimal.

Observed HIV prevalence was similar to that in Chongqing [10, 30] but much higher compared with Chengdu [29], Beijing [31], Shenzhen [32], and other cities in Jiangsu [33] and China [34, 35], whereas measured syphilis prevalence was much higher than previous observations in Jiangsu [36, 37], similar to Guangdong and Heibei, but higher than other places in China [37, 38].

Being located in the largest economic zone of eastern China, recent economic development has changed these 2 cities into the most active cruising areas for MSM engaged in high-risk sexual behaviors (multiple partners, frequent sex with female sex workers, injection drug use, etc), probably leading to an upsurge of STI epidemics [3], potentially indicating overall worsening of the HIV and syphilis situations in Jiangsu province, as sociodemographics in these 2 cities were quite similar to other cities in this province.

Whereas convenience sampling might have recruited [39] more high-risk MSM [10], stigma and social discrimination (associated with HIV/STIs [1], homosexuality, and bisexuality [40]) could also have influenced the upsurge of the epidemics by worsening the access of infected patients and MSM to prevention services [41].

Only about 30% of participants had higher education (24% in Yangzhou), much lower than previous observations [33, 34, 42].

Probably due to the sociocultural pressure [43], about half of the participants were married or had sex with women in the past 6 months. Among those, about 56% did not use condom at last vaginal intercourse, thus providing a platform for spread of HIV and syphilis from MSM to their female partners, revealing the potentially dangerous bridging role in these disease transmission [44].

As sex workers [45] and sadomasochist MSM engage in sexual practices associated with higher risk of STIs [46], increased risk of acquisition of HIV and syphilis among study subjects were likely, as 8.4% and 3.6% of them were engaged in commercial sex and sadomasochism, respectively, in the past 6 months.

Conducting 2 moderately large cohorts in 2 different cities with similar characteristics was the strength of this study. The overall large sample size provided considerably good power of the observed results and influence of the losses to follow-up was somewhat minimized. The use of biological markers of HIV and syphilis infection was also an important strength. The HIV RNA testing of each seronegative sample in the rapid test minimized the probability of misclassification of the outcome. All of the HIV-seropositive participants were referred to the standard care and treatment program run by the Chinese Center for Disease Control and Prevention. All diagnosed persons with syphilis were referred and treated at the STD clinic in our study sites.

Our study had some major limitations. The loss to follow-up, particularly between 6 months and 12 months, might have biased the results of our study. However, this was possible only if the loss to follow-up was differential (if the loss to follow-up was influenced by both exposure and outcome) [38]. It was possible that those who were lost to follow-up might have a higher incidence rate of HIV or syphilis than those who consistently participated, resulting in underestimation of the measures of occurrences of these 2 diseases. However, it was more likely that it was not associated with the outcome of interest, as would be the case if participants had been lost to follow-up because they actually migrated out of the study area due to their occupation or otherwise, resulting in nondifferential loss to follow-up, and hence might or might not have underestimated our results. Without additional information, we cannot conclusively predict the direction of the bias.

Other limitations of our study may include the short follow-up period (which spanned 12 months), self-reporting of the behaviors (which might have led to the misclassification of the variables of interest) of the participants, social desirability bias arising in face-to-face interviews regarding stigmatized behaviors, the use of convenience sampling strategy, and inadequate adjustment of potential confounders owing to lack of adequacy of the collected information.

Even with these limitations, we can still conclude that the HIV and syphilis incidence rates and prevalence were very high among participating MSM in the 2 cities of Jiangsu province, which raised the concern regarding potential rapid spread of HIV and syphilis among the MSM population of this part of China and probable transmission of these diseases to the general population. Urgent attention and effective intervention strategies are required to slow the epidemic of HIV and syphilis among MSM in the Jiangsu province of China.