Prevalence of Mycoplasma genitalium infection with antimicrobial resistance mutations among gay sex workers in China

Abstract

Background

Gay sex workers (GSWs) within the population of men who have sex with men in China are known as money boys (MBs). Limited research has been conducted to investigate the infection rate and antimicrobial resistance of Mycoplasma genitalium (M. genitalium) among GSWs in China. This study aimed to evaluate the status of M. genitalium infection among in GSWs.

Methods

This study was performed among 349 GSWs who were followed up for four years by internet-based sampling collection. The participants were asked to complete an online questionnaire using a mobile app, and trained interviewers took urethral, anorectal, and saliva swab specimens. STIs, including HIV and M. genitalium, were detected. Detection of resistance-associated mutations (RAMs) to macrolides and fluoroquinolones was performed via Sanger sequencing of the 23S rRNA, parC and gyrA genes.

Results

GSWs were enrolled by identifying 10 initial “seeds” from the Blued and WeChat apps. Face-to-face interviews were conducted with 349 GSWs from June 2017 to July 2021. The prevalence of M. genitalium and HIV positivity was 92/349 (26.4%, 95% confidence interval [CI] 21.7–31.0) and 71/349 (20.3%, 95% CI 16.3-24.4), respectively. The proportion of GSWs with M. genitalium infection alone in urethral swabs was 16, and the proportion with symptoms was 2/16 (12.5%). The proportion of GSWs with M. genitalium infection alone in anorectal swabs was 36, and the proportion with symptoms was 3/36 (8.3%). Multivariate regression analysis showed that using new types of drugs in the past 3 months and inconsistent condom usage with clients in the past 30 days were associated with M. genitalium infection. Macrolide resistance within the 23S rRNA gene was detected in 73/88 (83.0%) of the M. genitalium-positive GSWs. Moreover, 79.8% (71/89) of parC and 21.1% (19/90) of gyrA genes had mutations responsible for fluoroquinolone resistance. Three cases had no mutations in any of the three genes, 11 cases had mutations in all three genes, five cases had gyrA and parC gene mutations with no mutation in the 23S rRNA gene, and 42 cases had 23S rRNA and parC gene mutations with no mutation in the gyrA gene.

Conclusion

M. genitalium infections in our study displayed a high prevalence and very high levels of macrolide and fluoroquinolone resistance among GSWs in China. Asymptomatic M. genitalium infections are quite common among GSWs. Routine resistance testing of M. genitalium-positive specimens and antimicrobial resistance surveillance are crucial.

Keywords

prevalence men who have sex with men gay sex workers 23S rRNA

Introduction

In 2019, former United States President Donald J. Trump announced a goal for the reduction in the number of new HIV infections by 90% in the next 10 years (2030). This would be in addition to the $20 billion the US government already spends each year, domestically, for HIV prevention and care.¹ This foreseeable prevalence may be related to the preexposure prophylaxis (PrEP) and treatment as prevention (TasP) medication strategy adopted in recent years.² However, the implementation of this measure can lead to a decrease in condom use and increase the risk of other sexually transmitted infections (STIs).³ Men who have sex with men (MSM) are disproportionately affected by STIs, such as syphilis, Neisseria gonorrhoeae (NG), and Chlamydia trachomatis (CT).⁴ GSWs, as a subgroup of MSM who sell or exchange sex for money or goods, encompass a very diverse population across and within countries worldwide. In China, GSWs are known as money boys (MBs). China has approximately 380,000 MBs.⁵ Studies on GSWs in China are very limited, and GSWs are not included in routine HIV/STI surveillance.⁶

Accumulating evidence suggests that M. genitalium infection is an important bacterial STI. M. genitalium causes urethritis and cervicitis and potentially causes reproductive complications.⁷ The resistance of M. genitalium to first-line (azithromycin) and second-line (moxifloxacin) treatment has increased. The issue of drug resistance continues to attract the attention of the academic community.⁸ GSWs, as the bridge population of MSM,⁹ play a particularly important role in the process of M. genitalium transmission.¹⁰ However, studies on M. genitalium infection and drug resistance among GSWs are rare.

In recent years, the way GSWs recruit customers has undergone a fundamental change with the widespread use of mobile apps. WeChat is a Chinese multipurpose messaging, social media, and mobile payment app. Blued is a social media site with an app that originated in China for gay and bisexual men, transgender women, and MSM to communicate with each other to find sexual partners and share information.¹¹ Blued is currently the largest gay social network app in the world. We believe that this study is the first in China based on the Blued and WeChat apps to investigate the status of M. genitalium, HIV infection and drug resistance in the GSW population.

Methods

Volunteer recruitment and biological specimen collection

We recruited 349 GSWs from June 2017 to July 2021. A GSW was defined as any male who had provided sex services to other males for a fee within the previous 3 months. The inclusion criteria included the following: (1) males aged >18 years; (2) males who self-identified as a GSW; and (3) the ability to provide basic information and agree to specimen collection. At the beginning of the investigation, we identified 10 GSWs who had lived in Qingdao for a long time or stayed in Qingdao for a short time through an HIV-positive GSW named Mr. Yu. We trained the 10 seeds from March to May 2017 to master the item and research requirements. Seeds, their intermediaries, and every eligible peer they referred were given ¥300 CNY (equivalent to 44.28 USD, 41.02 EUR, 36.7 GBP).

In the following four years, our inspectors interviewed a total of 349 GSWs after introduction by the 10 seeds of GSWs. The locations included bars, nightclubs, motels, and temporary residences in seven cities in mainland China. During the interviews, we conducted an anonymous self-administered e-questionnaire through an online questionnaire in a mobile app; collected the interviewees’ age, occupation, monthly salary, number of male sexual partners, condom use with client, and other information; and collected urethral, anorectal, and oral swab specimens. The questions we designed for anogenital symptoms were as follows: Have you had any symptoms of urethral and anal discomfort in the past week? If the interviewees had symptoms of discomfort, they were further examined by the clinician immediately.

Specimen processing and sequencing

The use of these specimens for this evaluation was approved by the independent institutional review board of Qingdao Municipal Hospital. HIV testing was performed using oral fluid HIV self-tests (Rapid HIV-1/HIV-2 tests, Wondfo Technologies), and the results were not confirmed by blood-based specimen tests. Urethral and anorectal swab specimens were collected in duplicate using Ezup Saliva/Urine DNA Extraction Kits. CT, NG, M. genitalium, Mycoplasma hominis (MH), Ureaplasma urealyticum (UU), and Trichomonas vaginalis (TV) infections were detected by a Seeplex® STD6 ACE Detection kit.¹² The M. genitalium-positive specimens were further studied. All specimens were further studied for resistance associated mutations (RAMs) associated with the 23S rRNA gene within macrolides and the parC and gyrA genes within fluoroquinolones using previously published methods.¹³ Macrolide resistance can be caused by single-nucleotide mutations in the V region of the 23S rRNA gene at positions 2071 or 2072 (2058 or 2059 in Escherichia coli numbering). Fluoroquinolone resistance is caused by mutations resulting in amino acid changes within the known RAMs within the gyrA and parC genes. PCR amplification was performed by Sanger sequencing.

Statistical analysis

Data from the online questionnaire and laboratory test results were analysed using SPSS 22.0 (SPSS, Inc., Chicago, IL, USA) software. Our analysis showed that the measurement data in this study were not normally distributed. Therefore, the measurement data were expressed as medians (quartiles), and the count data were expressed as frequencies (percentages). Odds ratios (ORs) including 95% confidence intervals (CIs) were used. The data were analysed using the chi-squared test. Risk factor analysis of M. genitalium infection was performed using univariate and multivariate logistic regression analyses. The forwards stepwise method was used to select the variables that were eventually included in the model. Variables that showed statistical significance (P < 0.1) in the univariate analysis were included in the multivariate logistic regression analysis. Forest plots were plotted by https://www.bioinformatics.com.cn (last accessed on 31 Oct 2021), an online platform for data analysis and visualization.

Results

Population characteristics and M. genitalium infection risk factors

A total of 349 GSWs were enrolled in this research from June 2017 to July 2021. The median age of the cohort was 24 years (range, 18–46 years). Most of the participants identified their sexual orientation as homosexual (250/349, 71.6%), bisexual (88/349, 25.2%), or transgender (11/349, 3.2%). Half of the participants (182/349, 52.1%) worked full time. Only 48 (13.8%) of the GSWs had an education level of college or above. More than half (187/349, 53.6%) had a monthly income that exceeded 20,000 CNY. Approximately 57.9% of the GSWs participated in group sex activities, 21.2% used new drugs in the past 3 months, and 49.9% received more than 20 guests in the past 30 days. The total prevalence of HIV positivity among GSWs was 20.3% (71/349). Of the 51 respondents who were followed up by WeChat, only 5 had new positive results. We recommended that these individuals visit their local CDC for further confirmatory testing. Approximately 64.2% of the GSWs reported consistent condom usage with clients in the past 30 days, 74.2% had no preferred sexual roles, 14.6% suffered STIs in the past 12 months, 9.7% suffered physical violence in the past 6 months, and 22.9% had suicidal thoughts. Details are shown in Supplementary Table S1.

Univariate analysis showed that the statistically significant risk factors associated with M. genitalium infection were group sex in the past 3 months, using new types of drugs in the past 3 months, and consistent condom usage with clients in the past 30 days. Five independent risk factors (P < 0.1) screened from the univariate analysis were included in the multivariate logistic regression. Multivariate logistic regression showed that using new types of drugs in the past 3 months (OR: 1.870, 95% CI: 1.083−3.232) and inconsistent condom usage with clients in the past 30 days (OR: 1.747, 95% CI: 1.062−2.874) were significantly associated with M. genitalium infection. Details are shown in Figure 1 and Supplementary Table S1.

Table 1.

Frequency of Mutations Identified in the 23S rRNA, parC, and gyrA Genes. According to (Machalek DA, 2020).

Gene	Position and Mutation	Amino acid change	No.of samples
gyrA	G240A	No change	1
	G285A	Met95Ile	13
	G285T	Met95Ile	1
	G295A	Asp99Asn	2
	G295T	Asp99Tyr	1
	A296G	Asp99Gly	1
	WT		71
	Unavailable sequencing		2
parC	C234T	No change	1
	G248A	Ser83Asn	2
	G248T	Ser83Ile	65
	G259T	Asp87Tyr	2
	C324T	No change	1
	WT		18
	Unavailable sequencing		3
23S rRNA	A2058G	NAAP	11
	A2059T	NAAP	14
	A2059C	NAAP	9
	A2059G	NAAP	39
	WT	NAAP	15
	Unavailable sequencing		4

Abbreviations: WT, wild type; US, unavailable sequencing; NAAP: No amino acid product.

Prevalence of M. genitalium infection and other STIs

Among the 349 GSWs, 92 (26.4%, 95% CI 21.7–31.0) had M. genitalium infection in any site; 65 (70.7% [95% CI: 62.0%–80.4%]) had M. genitalium infection in the rectum; 41 (44.6% [95% CI: 34.8%–54.3%]) had M. genitalium infection in the urethra; and 14 (15.2% [95% CI: 8.7%–22.8%]) had M. genitalium infection in two sites. The proportion of GSWs with M. genitalium infection alone in urethral swabs was 16, and the proportion with symptoms was 2/16 (12.5%); the proportion of GSWs with M. genitalium infection alone in anorectal swabs was 36, and the proportion with symptoms was 3/36 (8.3%). C. trachomatis was detected in 19/92 (20.7%) GSWs at any site, N. gonorrhoeae was detected in 14/92 (15.2%) GSWs at any site, T. vaginalis was detected in 3/92 (3.3%) GSWs at any site, U. urealyticum was detected in 15/92 (16.3%) GSWs at any site, and M. hominis was detected in 4/92 (4.3%) GSWs at any site. Details are shown in Supplementary Table S2.

Prevalence of resistance mutations

Among the 92 available specimens that tested positive in M. genitalium sequencing, 97.6% (40/41), 100% (41/41), and 97.6% (40/41) had successful sequencing of 23S rRNA, parC, and gyrA genes in urethral specimens, respectively, and 95.4% (62/65), 95.4% (62/65), and 98.5% (64/65) had successful sequencing of 23S rRNA, parC, and gyrA genes in rectal specimens, respectively. Among the 14 specimens of both sites, the results of gene sequencing showed that the genotypes were consistent. The proportion of RAMs to macrolides with the 23S rRNA gene was detected in 83.0% (73/88) of specimens at all sites, and the most common mutation was A2059G (n = 39), followed by A2058T (n = 14), A2058G (n = 11), and A2059C (n = 9), according to E. coli numbering. The rate of possible fluoroquinolone RAMs in parC mutations was 77.5% (69/89). The most frequent parC QRDR amino acid alterations were g248t (n = 65), g248a (n = 2), and g259t (n = 2). The rate of possible fluoroquinolone RAMs in gyrA mutations was 20% (18/90). The most frequent amino acid alterations in gyrA were g285a (n = 13), g295a (n = 2), a296g (n = 1), g285t (n = 1), and g295t (n = 1). Three of ninety-two M. genitalium specimens expressed no RAMs to either antimicrobial. Details are shown in Supplementary Table S1.

Discussion

This study is the first large-scale prospective evaluation in China to determine M. genitalium infection among GSWs. We found that apps have become the predominant route to seek male clients, and the prevalence of M. genitalium and HIV positivity in this subgroup is high.

The 349 GSWs investigated had a high HIV-positive rate of 20.3%. Growing evidence indicates a sustained or increasing burden of HIV among GSWs.¹⁴ M. genitalium infection is a bacterial STI with a prevalence second only to C. trachomatis in most studies.¹⁵ The prevalence of M. genitalium infection in the general population varies between 1–3%.¹⁶ The prevalence of M. genitalium among GSWs in the present study was more than five times the national average among MSM (26.4% vs. 5.0%).¹⁶ A contemporary study in Shenyang city, China, found that the infection rate of M. genitalium among MSM is 15.3%,¹⁷ which is lower than the 26.4% in the current study. The prevalence of M. genitalium among female sex workers is 10.8% in Belgium,¹⁸ 12.9% in Nairobi,¹⁹ and 14.1% in Japan.²⁰ To our knowledge, this study is the first to report on the infection rate of M. genitalium among GSWs. Notably, most individuals whose anal or urethral specimens were positive for M. genitalium were asymptomatic. This finding is consistent with the results of Read.²¹ Thus, M. genitalium infection is likely to be widely underdiagnosed. We found that the infection was remarkably more common in the rectum than in the urethra (55.4% vs. 29.3%). These findings have been replicated in several other studies in different MSM populations.^22,23

According to the risk analysis of M. genitalium infection, inconsistent condom usage with clients in the past 30 days and drug use are high-risk factors for M. genitalium infection. Studies on the risk factors for STIs had different results because of differences in the questionnaires used. A prior report on 490 female sex workers showed that noncondom use was not associated with STIs. Independent risk factors included participation in group sex.²⁴ Cara et al.²⁵ also found that group sex behaviours among MSM were related to STIs. Ample evidence shows that the use of new drugs can also increase the risk of STIs.^26–28

In this research, macrolide resistance was detected in 83.0% (73/88) of the M. genitalium-positive individuals, and 77.5% (69/89) of parC and 20% (18/90) of gyrA genes had mutations responsible for fluoroquinolone resistance. All mutations detected in this study have been described previously. Our findings of high macrolide and fluoroquinolone resistance rates in M. genitalium implied that the use of azithromycin and moxifloxacin as empirical first- and second-line therapies, respectively, might be ineffective.

A meta-analysis found that the prevalence of mutations associated with macrolide resistance worldwide is 51.4%, and the prevalence of fluoroquinolone resistance in M. genitalium specimens is 7.7%.²⁹ A study of male and female patients who sought care at an STI clinic in Guangzhou, China, from 2016 to 2018 showed that 66.4% (101/152), 0.7% (1/147) and 77.7% (108/139) of samples manifested mutations in the 23S rRNA, gyrA and parC genes, respectively.³⁰ The latest data from the same region show that the rRNA gene had a mutation rate of 64% in 23S, and that of the parC gene was 67.5%.³¹ The above data show no significant change in the mutation rate. A survey of male patients with STIs in Hong Kong, China, showed that the mutation rate of 23S rRNA was 47% and that of parC was 53%.³² An Australian study among 742 asymptomatic MSM showed the presence of macrolide resistance in 75.0% of infections.³³ A French study found that the overall rates of M. genitalium resistance to macrolides and fluoroquinolones were 67.6% and 9.1%, respectively, among MSM.³⁴ A survey in Germany in HIV-positive MSM showed that resistance-associated mutations to macrolides and fluoroquinolones were found in 60% and 30% of cases, respectively.³⁵ In summary, MSM, as a special population, have a high mutation rate of M. genitalium-related genes compared with the general population. GSWs in this study showed a higher mutation rate than general MSM.

Prostitution is illegal in China; thus, GSWs represent a subset of individuals who have been mostly ignored and are hard to reach for STI monitoring. Therefore, many public health questions about GSWs are poorly studied. Unfortunately, public and private funders are reducing investments in HIV and STI prevention and control in mainland China. Apps are an ideal way to seek clients. GSWs use apps as the only way to seek clients; thus, investigations among this group of people are extremely difficult. Although few studies and scant systematic surveillance have been conducted on the burden of M. genitalium among these men, the evidence of this study indicates that M. genitalium infections and high levels of RAM rates in this population remain.

This study had several limitations. First, the method used in this research was the snowball method, which could be affected by population selection bias. Eight of the 10 seed GSWs were HIV-positive men, which may have led to population selection bias among the respondents. Second, the subjects were also evaluated for their information leakage risk, which might have led to an underreporting of various factors, such as drug use and participation in group sex.

Conclusion

Mobile apps, particularly Blued, have become the main way for GSWs to find customers. The WeChat app is also an important way for GSWs to attract customers. HIV and M. genitalium infections were highly prevalent in our study. The levels of macrolide and fluoroquinolone resistance among GSWs in China are very high. GSWs are likely to be a reservoir of STI agents, and it is highly important to include them in surveillance programs.

Supplemental Material

Supplemental Material - Prevalence of Mycoplasma genitalium infection with antimicrobial resistance mutations among gay sex workers in China

Supplemental Material for Prevalence of Mycoplasma genitalium infection with antimicrobial resistance mutations among gay sex workers in China by Lixin Wang, Zhi Li, Chuan Wan, Xuanxuan Tian, Hongye Liu, and Yang Li in International Journal of STD & AIDS.

Supplemental Material

Supplemental Material - Prevalence of Mycoplasma genitalium infection with antimicrobial resistance mutations among gay sex workers in China

Footnotes

Acknowledgements

The authors would like to thank all the staff and participants who joined in this study for their time spent on this project, especially “Mr. Yu,” whose full participation and coordination made this research possible. We acknowledge the contribution and support of the AZURE Working Group, without whom this work would not have been possible. We did not provide the full names of group members because of personal privacy issues.

Declaration of Conflicting Interests

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

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical approval

All participants gave verbal informed consent prior to participation in this study. Each participant was clearly informed that he could decline or withdraw from the survey at any time. The e-questionnaire was kept under a specific account, which was inaccessible to anyone but research staff. The study protocol and consent were approved by the Ethics Review Committee of the Affiliated Qingdao Municipal Hospital of Qingdao University (Ethical Review [2017] No. 006).

ORCID iD

Yang Li

Supplemental Material

Supplemental material for this article is available online.

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Supplementary Material

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