Abstract

Background

Chlamydia and gonorrhea notifications are rapidly rising in men who have sex with men (MSM). Currently, there are limited data on the prevalence of chlamydia and gonorrhea across various anatomical sites. Our study aimed to explore the prevalence, association and changing trends of urethral and rectal chlamydia and gonorrhea among MSM in Guangdong Province, China.

Methods

We analyzed data among MSM attending sexually transmitted infections (STI) clinics in the Guangdong governmental sentinel network between 2018 and 2022. Chi-square tests were used to compare the difference, Join-point regressions for analyzing changing trends, and multivariate logistic regressions for examining associated factors.

Results

We included 4856 men in the analysis. Rectal chlamydia significantly increased from 13.8% to 26.4% over the past 5 years (average annual percentage change [AAPC] 19.2%, 95%CI 1.0-40.6, p = 0.043). After adjusting for covariates, chlamydia infection positively associated with main venue used to seek sexual partners (aOR = 2.31, 95%CI 1.17–4.55), having regular sexual partners in the past 6 months (aOR = 3.32, 95%CI 1.95–5.64), receiving HIV counselling and testing services (aOR = 2.94, 95%CI 1.67–5.17), receiving peer education (aOR = 1.80, 95%CI 1.14–2.83), infection with syphilis (aOR = 2.02, 95%CI 1.02–4.01) and infection with gonorrhea (aOR 7.04, 95% CI 3.01–16.48). Gonorrhea infection positively associated with having regular sexual partners in the past 6 months (aOR = 3.48.95%CI 1.16–10.49), and infection with chlamydia (aOR 7.03, 95% CI 2.99–16.51).

Conclusions

To conclude, our findings reveal a high prevalence of chlamydia infections among MSM, particularly in the rectal area. Comprehensive chlamydia and gonorrhea health services are necessary for MSM to improve sexual health.

Introduction

Chlamydia and gonorrhea are the two most pervasive and curable sexually transmitted infections (STI) worldwide. Approximately 82Ìýmillion new cases of gonorrhea and 129Ìýmillion cases of chlamydia occurred in 2020 [1]. World Health Organization (WHO) estimated that, in 2016, the global prevalence of chlamydia and gonorrhea in 15-49-year-old men was 2.7% and 0.7%, respectively [2]. Men who have sex with men (MSM) are disproportionately affected by chlamydia and gonorrhea, which contributing substantially to the worldwide infection burden [2]. In China, the prevalence of chlamydia and gonorrhea infections among MSM in 2018 ranged from 13.9 to 22.5%, and 5.3 to 11.0%, respectively [3,4,5].

Previous studies showed that the prevalence of chlamydia and gonorrhea varied in different anatomical sites among MSM [5]. A literature review reported that the global prevalence among MSM was 2.1-23% for rectal chlamydia, 0-3.6% for pharyngeal chlamydia, 0.2–24% for rectal gonorrhea, and 0.5-16.5% for pharyngeal gonorrhea [6]. Studies conducted among MSM in China [3, 5], Netherlands [7], the United States [8], Germany [9], and Thailand [10, 11] have found that rectal chlamydia and gonorrhea infections were more common than urethral infections and more likely to be asymptomatic [3,4,5,6,7,8,9,10,11,12,13,14]. Routine screening for rectal chlamydia and gonorrhea is recommended in many countries such as the United States, Australia, and the United Kingdom [12, 15]. But in China, there is currently no national policy specifically guiding rectal chlamydia and gonorrhea screening for MSM, and only the China Chlamydia Intervention Programme Implementation Plan (2021) recommends biannual screening based on self-reported sexual positioning in selected pilot regions [16]. As widespread stigma and societal pressures, MSM may feel the need to conceal their sexual behaviors, potentially leading to missed opportunities for rectal screening [17]. These undiagnosed chlamydia and gonorrhea infections are a potential reservoir for ongoing transmission in MSM and may also lead to increased risk of human immunodeficiency virus (HIV) acquisition [18]. Thus, there was a need to inform planning of intervention programs and related policy updates to ensuring that a greater number of MSM are reached and more infections are identified. However, data on the prevalence of chlamydia and gonorrhea in different anatomic sites among Chinese MSM was still limited [13, 19].

Therefore, we conducted this study to explore the prevalence, association and changing trends of urethral and rectal chlamydia and gonorrhea infections among Chinese MSM by using sentinel surveillance data from 2018 to 2022 in Guangdong, China.

Methods

Guangdong governmental sentinel surveillance network

Guangdong Province is located in southern China, which comprises of 21 cities and with a large population. Over the past decade, Guangdong has the largest number of STI cases in China, and has been among the top three provinces with the highest reported chlamydia and gonorrhea incidence which have consistently risen over time [20, 21].

Under the growing epidemic of chlamydia and gonorrhea in Guangdong, a Guangdong governmental sentinel surveillance network among MSM was established in 2018 comprising four cities (Shenzhen, Yunfu, Jiangmen, and Foshan). These four cities were selected because of high burden of STIs and better local capacity. A standardized sentinel survey protocol designed by the Guangdong Provincial Centre for STI Control was sent to sentinel surveillance network sites for data collection and management. It was conducted routinely for data and samples collection by the local STI hospital from April to August each year since 2018.

In each surveillance site, outreach teams were set up and comprised of clinical physicians, nurses, and public health physicians from local STI clinic. They have extensive experience to provide comprehensive public health services and risk reduction for MSM, including condom promotion, STI testing, sexual health education, and behavioral intervention. Participants in this surveillance were recruited using convenience sampling at MSM event venues by outreach teams from pub, disco, tea room and club through offline outreach services. As a rule of thumb and based on the recommendation of WHO and prior sentinel surveillance in Guangdong [20, 22, 23], a minimum sample size of 250 participants was required for each sentinel surveillance site. According to the surveillance protocol, the eligible criteria of participants included born biologically as male, more than 18-year-old, and had oral or anal sex with a man at least once in the past 6 months.

Data collection

The sentinel surveillance program annually collected information including sociodemographic characteristics, sexual behaviors, illicit drug use and testing history among MSM in each surveillance site. The data were collected using paper questionnaires (Supplementary material p 2) in this study. The questionnaire items were determined based on the discussions with STI experts, MSM, and outreach service staff. To pretest feasibility of questionnaire items and proficiency of outreach teams, a pilot survey was conducted among 20 volunteer MSM. The data from pilot survey were excluded from the final analysis. Eligible individuals who agreed to participate in the study were asked to provide written informed consents, and then invited to a separate and private room to complete a questionnaire with the help of a trained stuff. In order to notify the testing results, we collected the phone number of each participant.

Measure

Socio-demographic and behavioral variables

Socio-demographic characteristics included age, marital status, educational level, household registration (Guangdong province/other provinces) and ethnicity. Sexual behavioral variables included the following: any anal sex with men in the past 6 months, consistently condom use during anal sex in the last 6 months, main venue where MSM used to seek sexual partners, any regular sexual partners in the past 6 months, whether received HIV counselling and testing services, and whether received peer education. Consistently condom use was defined as using condoms during every anal sex in the past 6 months. Main venue where MSM used to seek sexual partners including websites, bars, disco, tearooms, bathrooms, parks and so on. Illicit drug use was defined as using any of the following drugs in the past year, including cannabis, heroin, cocaine, crack, ecstasy, amphetamines, poppers, keta-mine and methamphetamine. Testing history included previous testing for chlamydia, gonorrhea, HIV, syphilis, and Hepatitis C virus (HCV) in the past 6 months.

Laboratory testing for STIs

After completing the questionnaire, all participants were instructed to collect urine samples by themselves, while blood and anal swab samples were collected by the staff at each outreach service site. Urine samples were collected for chlamydia and gonorrhea testing, while anal swabs were only collected from those who engaged in receptive anal sex in the past 6 months regardless of using condoms. All urine and anal swabs samples were transported to the Southern Medical University Dermatology Hospital for laboratory testing using the Cobas 4800 CT/NG detection kits (Roche Moleculer Systems, Inc. New Jersey, USA). The results of urine tests and anal swabs were returned to each surveillance site in 2 weeks after receiving the samples. All blood samples were analyzed at local STI clinics and tested for HIV using enzyme-linked immunoassay (ELISA, Lizhu Biotech Inc, Zhuhai, China), for syphilis using the rapid plasma reagin test (RPR, Lizhu Biotech Inc, Zhuhai, China) and Treponema pallidum particle agglutination test (TPPA, Rongsheng Biotech Inc, Shanghai, China), and for HCV using enzyme-linked immunosorbent assay (ELISA, Wantai Biotech Inc, Beijing, China). In our study, syphilis positive was defined as both RPR and TPPA positive. Positive test results for HIV, syphilis and HCV antibodies were conveyed to MSM via text messages within one week. Following this, the local outreach team extended referral services to guide MSM in accessing prompt and appropriate treatment. Post-test counselling and appropriate medical care for HIV, STI, and HCV was implemented according to standard STI clinic procedure [24].

Data analysis

To establish a database, questionnaire data and laboratory results in this study were double-entered to Epidata software (EpiData Association from Denmark) and data consistency check was conducted to deal with data errors, data loss, and data duplication.

The sociodemographic characteristics and sexual behaviors were presented as number and percentage using descriptive analysis by survey year. Chi-square test was used to compare differences of sociodemographic characteristics and sexual behaviors by years. In addition, Join-point regression was used to identify changing trends of chlamydia and gonorrhea prevalence by anatomic sites as well as HIV, syphilis, and HCV from 2018 to 2022. It estimated the average annual percentage change (AAPC) with 95% Confidence interval (CI) in the whole period. Univariate and multivariate logistic regressions were conducted to explore the factors associated with chlamydia and gonorrhea infections among MSM. As participants may repeatedly involve in this active surveillance across different years, we analyzed data only from the most recent survey year (2022) for associated factor analysis to avoid duplicate samples. In the multivariate model, we adjusted for age, legal marital status, highest level of education, household registration, and ethnicity. These adjusted variables were selected based on our previous experience [13, 20, 25, 26]. Significance was defined at p-value < 0.05. All analyses were conducted on SPSS 25.0, and Join-point regression was conducted on Join-point regression Program, Version 4.9.1.0 (Statistical Research and Applications Branch, National Cancer Institute).

Results

Sociodemographic and sexual behavior characteristics

A total of 4856 men were recruited for this study, including 893 in 2018, 959 in 2019, 1009 in 2020, 1008 in 2021, and 987 in 2022. Most of the men were characterized as being younger than 40 years old (range from 65.3% in 2019 to 72.0% in 2022), unmarried (range from 63% in 2018 to 68.2% in 2022), having a high school degree or above (range from 73.4% in 2019 to 81.7% in 2021), with household registration in Guangdong Province (range from 56.6% in 2022 to 67.3% in 2019). During the past 6 months, most men engaged in anal sex with men (range from 82.5% in 2018 to 93.8% in 2021). About three-fifths of men used condom consistently during the past 6 months (range from 59.8% in 2018 to 81% in 2019). Only few participants had ever tested for chlamydia (range from 3.6% in 2018 to 11.9% in 2020) and gonorrhea (range from 3.8% in 2018 to 11.4% in 2020). (TableÌý1)

Table 1 Sociodemographic and sexual behaviors characteristics of MSMs in Guangdong province, 2018–2022

Trends of chlamydia and gonorrhea prevalence

The prevalence of chlamydia infection among MSM remained stably high between 2018 and 2022, ranging from 8.6 to 9.4% (AAPC = 5.4%, 95% CI -10.3 to 24.0, p = 0.375). The prevalence of urethral infection dropped from 5.5% in 2018 to 3.4% in 2022 (AAPC=-9%, 95% CI -37.3-32.1, p = 0.478), while the co-infection rate at both urethral and rectal sites rose from 2.1% in 2018 to 3.3% in 2022 (AAPC = 11.0%, 95% CI -28.7-72.7, p = 0.507), although neither trend was significant. By contrast, among MSM who provided anal swabs, the infection rate at the rectal site showed a significant increasing trend from 13.8% in 2018 to 26.4% in 2022 (AAPC = 19.2%, 95% CI 1.0-40.6, p = 0.043). (TableÌý2; Fig.Ìý1)

Table 2 Prevalence of chlamydia and gonorrhea infection by anatomic sites among MSM in Guangdong Province, 2018–2022

Fig. 1

Prevalence of chlamydia by anatomic sites in Guangdong Province,2018–2022

The prevalence of gonorrhea infection also remained fairly stable between 2018 and 2022, ranging from 3.4 to 2.5% (AAPC = 1.0, 95% CI -26.7 to 39.2, p = 0.926). During the five-year study period, the prevalence of urethral or rectal infections declined from 2.1 to 1.4% (AAPC = -2.6%, 95% CI -31.9 to 39.3, p = 0.832) and from 5.0 to 4.5% (AAPC = 0.8%, 95% CI -40.2 to 70.0, p = 0.962), respectively, but these decreases were not significant. The co-infection rate of urethral and rectal gonorrhea ranged from 0.0 to 1.1% during 2018–2022. (TableÌý2; Fig.Ìý2)

Fig. 2

Prevalence of gonorrhea by anatomic sites in Guangdong Province,2018–2022

In the study period, prevalence of HIV, syphilis, and HCV infections among MSM did not change significantly. HIV prevalence dropped from 7.3% in 2018 to 5.0% in 2022 (AAPC = -15.0, 95% CI -35.7 to 12.3, p = 0.160), and syphilis prevalence decreased from 11.9% in 2018 to 8.5% in 2022 (AAPC = -16.4, 95% CI -57.3 to 63.9, p = 0.459). HCV prevalence was 0.2% in 2018, 0.1% in 2019, 0.1% in 2020, and 0.2% in 2022. (TableÌý2)

Factors associated with chlamydia and gonorrhea

In multivariate analysis, after adjusting for age, education level, marital status, household registration and ethnicity, chlamydia infection in 2022 was positively associated with the following factors: main venue used to seek sexual partners (aOR = 2.31, 95%CI 1.17–4.55), having regular sexual partners in the past 6 months (aOR = 3.32, 95%CI 1.95–5.64), receiving HIV counselling and testing services (aOR = 2.94, 95%CI 1.67–5.17), receiving peer education (aOR = 1.80, 95%CI 1.14–2.83), infection with syphilis (aOR = 2.02, 95%CI 1.02–4.01) and infection with gonorrhea (aOR = 7.04, 95% CI 3.01–16.48). Gonorrhea infection in 2022 was positively associated with having regular sexual partners in the past 6 months (aOR = 3.48, 95%CI 1.16–10.49), and infection with chlamydia (aOR = 7.03, 95% CI 2.99–16.51). (TableÌý3)

Table 3 Factors associated with gonorrhea and chlamydia infections among MSM in Guangdong Province,2022. (N = 987)

Discussion

This study has yielded the following significant findings. First, our research identifies a consistent and high prevalence of chlamydia and gonorrhea among Chinese MSM from 2018 to 2022. Second, our findings suggest that the rectum infection were common among MSM, with a significant increasing trend in rectal chlamydia infections over the five-year period. Third, this study indicated low levels of testing for chlamydia and gonorrhea among MSM in China. This study expands the limited literature by focusing on a low- and middle-income countries (LMIC) context, including longitudinal data over a 5-year period, assessing chlamydia and gonorrhea infections at different anatomical sites among MSM, and exploring associated factors. Findings from this study can help inform the development of interventions for chlamydia and gonorrhea among MSM in China.

This study found that from 2018 to 2022, the overall prevalence of chlamydia infection among MSM has consistently remained at a high level, exceeding that reported by MSM sentinel surveillance in Australia (6.2%) [27]. Multiple factors are probably at play, including MSM multiple risk sexual behaviors, mobility of the MSM population, and the limited funding and control measures for chlamydia [4]. Compared to the HIV and syphilis prevention and control strategies, there is a lack of national control guidelines or prevention programs specifically targeting chlamydia prevalence in China; And chlamydia in China is not routinely reported as a notifiable infectious disease into the national surveillance program [28]. Preventive services for vulnerable groups such as MSM are also very limited. In high-income countries like Australia and the United States, comprehensive STI/HIV prevention, treatment, and care services tailored specifically for MSM are widely available [29, 30]. Incorporating comprehensive chlamydia and gonorrhea health services into existing STIs/HIV prevention programs, and providing accessible prevention services and counseling support for MSM should be considered, which can ensure equitable access to essential healthcare services and support, leading to a reduction in infections among this population.

Our surveillance data revealed a significantly increase prevalence of rectal chlamydia among MSM from 2018 to 2022. The increasing trend in the rectal infection rates could be partly attributed to a widely performed screening of rectal sites in the sentinel surveillance implementation in recent years in China, as well as the increased awareness among clinicians and the adoption of more sensitive and specific testing methods, leading to an increase in reported cases [31]. Furthermore, increasing rectal chlamydia rates could also be related to the reduction in facility-based testing due to COVID-19. Healthcare providers and systems likely prioritized testing symptomatic patients during this period deferring routine preventive health appointments that include asymptomatic STI screenings [32]. As chlamydia urethritis is generally less severe than gonorrhea urethritis, less asymptomatic screening during the pandemic probably led to more undiagnosed chlamydia urethritis cases and subsequently to onward transmission to the rectum. Regular rectal testing targeting sexually active MSM are needed. However, some barriers may impede access to and the uptake of rectal screening services among MSM. Firstly, asymptomatic infections are more prevalent in the rectal site compared to the urethral site, leading to a lack of awareness among infected MSM about the necessity of testing and treatment [6]. Additionally, in many LMIC, chlamydia and gonorrhea are primarily managed based on symptomatic presentations [33]. Lastly, the fear of invasive sampling methods also hinders MSM seeking rectal testing services [34, 35]. In our study, only a few participants opted for anal swabs, despite the availability of this testing method at all surveillance sites. Thus, healthcare providers should proactively inquire about MSM’s sexual history and encourage them to undergo rectal testing, especially for those engaging in anal sexual behaviors [11, 34]. Furthermore, further studies are needed to identify factors that influence the acceptability of rectal testing among MSM and explore innovative methods to enhance its uptake.

This study found that the uptake of chlamydia and gonorrhea testing among MSM remained consistently low between 2018 and 2022. The proportion of MSM who reported ever being tested for chlamydia and gonorrhea in our study was lower compared to proportion reported in the USA (45.9-81.4% for chlamydia, 50.4-83.9% for gonorrhea) [8]. Currently, testing for chlamydia and gonorrhea in China remains health facility-based. Accessing facility-based testing services may be challenging for MSM due to social stigma, discrimination, and fear of being ostracized because of their sexual behaviors [34]. Furthermore, over half of the study period coincided with the COVID-19 pandemic, and the implementation of related lockdown measures likely disrupted the provision and access to STIs testing services [36]. A study investigating the impact of COVID-19 on HIV testing in China revealed a 59% reduction in facility-based testing among MSM during the pandemic [37]. Innovative testing strategies in non-clinical settings (e.g., Internet-based self-sampling, postal self-sampling and home-based self-test) can offer opportunity and confront the structural barriers to chlamydia and gonorrhea testing for MSM [28, 35, 38]. Expanding the implementation of novel testing approaches and creating MSM-friendly environments for MSM could be considered to promote testing uptake among MSM in the future.

We recognized several limitations of the study. First, because we did not collect pharyngeal swabs, we were unable to evaluate the prevalence of pharyngeal chlamydia and gonorrhea. According to previous research, gonorrhea is more common in the pharynx and can be a reservoir for antibiotic resistance due to the potential exchange of genetic material between NG and other commensals of this niche, including other Neisseria species [15, 39,40,41]. Second, we did not ask the participants whether they had any symptoms, so we cannot determine the prevalence of asymptomatic infections. Third, the cross-sectional study design cannot illustrate the causality between associated factors and recent chlamydia and gonorrhea infection. Last, the susceptibility of the self-reported behavioral data to social desirability bias, which might introduce information bias. Additionally, rectal swabs were collected only from men who reported engaging in anal intercourse within the past 6 months, the number of MSM infected with rectal infection might be underestimated. Rectal testing also relying on voluntary participation might introduce self-selection bias leading to an overestimate of the prevalence of rectal infection.

Conclusions

In conclusion, our findings reveal a high prevalence of chlamydia infections among MSM, particularly in the rectal area. More targeted intervention chlamydia and gonorrhea prevention strategies and efforts, such as early detection, development of new diagnostics and novel treatment options, should be paid more attention in the future.