Article Text
Abstract
Background Meeting sex partners online is associated with increased risk of acquiring sexually transmitted infections. We examined whether different venues where men who have sex with men (MSM) meet sex partners was associated with prevalent Chlamydia trachomatis (CT) and Neisseria gonorrhoeae (NG) infection, and whether prevalence increased during (vs before) the COVID-19 pandemic.
Methods We conducted a cross-sectional analysis of data from San Diego’s ‘Good To Go’ sexual health clinic from two enrolment periods: (1) March–September 2019 (pre-COVID-19) and (2) March–September 2021 (during COVID-19). Participants completed self-administered intake assessments. This analysis included males aged ≥18 years self-reporting sex with males within 3 months before enrolment. Participants were categorised as (1) meeting new sex partners in-person only (eg, bars, clubs), (2) meeting new sex partners online (eg, applications, websites) or (3) having sex only with existing partners. We used multivariable logistic regression, adjusting for year, age, race, ethnicity, number of sex partners, pre-exposure prophylaxis use and drug use to examine whether venue or enrolment period were associated with CT/NG infection (either vs none).
Results Among 2546 participants, mean age was 35.5 (range: 18–79) years, 27.9% were non-white and 37.0% were Hispanic. Overall, CT/NG prevalence was 14.8% and was higher during COVID-19 vs pre-COVID-19 (17.0% vs 13.3%). Participants met sex partners online (56.9%), in-person (16.9%) or only had existing partners (26.2%) in the past 3 months. Compared with having only existing sex partners, meeting partners online was associated with higher CT/NG prevalence (adjusted OR (aOR) 2.32; 95% CI 1.51 to 3.65), while meeting partners in-person was not associated with CT/NG prevalence (aOR 1.59; 95% CI 0.87 to 2.89). Enrolment during COVID-19 was associated with higher CT/NG prevalence compared with pre-COVID-19 (aOR 1.42; 95% CI 1.13 to 1.79).
Conclusions CT/NG prevalence appeared to increase among MSM during COVID-19, and meeting sex partners online was associated with higher prevalence.
- COVID-19
- Chalmydia trachomatis
- gonorrhea
- sexual and gender minorities
Data availability statement
Data are available on reasonable request. De-identified participant data are available through the UC San Diego Antiviral Research Center (UCSD AVRC) by emailing the database administrator, Tara Tenenbaum, at tchaloukian@ucsd.edu.
This article is made freely available for personal use in accordance with BMJ’s website terms and conditions for the duration of the covid-19 pandemic or until otherwise determined by BMJ. You may use, download and print the article for any lawful, non-commercial purpose (including text and data mining) provided that all copyright notices and trade marks are retained.
https://bmj.com/coronavirus/usageStatistics from Altmetric.com
WHAT IS ALREADY KNOWN ON THIS TOPIC
Meeting sex partners online is associated with a higher prevalence of sexually transmitted infections; however, this is the first paper to our knowledge that examines how meeting sex partners and the prevalence of Chlamydia trachomatis (CT)/Neisseria gonorrhoeae (NG) changed during the COVID-19 pandemic, compared with before.
WHAT THIS STUDY ADDS
The prevalence of CT and NG increased during the COVID-19 pandemic, while many sexual behaviours decreased.
This further adds to current literature by showing that the odds of CT and NG infection were increased among men who have sex with men (MSM) who met sex partners online.
HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE OR POLICY
Policies and interventions are needed to address events, such as the COVID-19 pandemic, which produce barriers and possible disruptions in sexual health services for MSM.
Introduction
Men who have sex with men (MSM) are disproportionately impacted by sexually transmitted infections (STIs), particularly at extragenital sites for Chlamydia trachomatis (CT) and Neisseria gonorrhoeae (NG).1 For example, the prevalence of rectal NG and CT can be as high as 24% and 23%, respectively.1 It is estimated that approximately 70% of NG and CT infections are asymptomatic, thereby posing a concern during the COVID-19 pandemic when asymptomatic screening may have declined due to clinics limiting appointments to only patients experiencing symptoms.1 2
Transmission of STIs can vary by where MSM meet sex partners, such as in-person venues (ie, bars, clubs, gyms or other physical locations frequented by MSM), through online venues (ie, websites or mobile applications) or by maintaining existing sex partners.3 Research that predates the pandemic has shown an increase in odds of NG and CT among MSM who meet sex partners online.4 5 Specifically, one study identified increased odds of CT and NG among those who met sex partners online and in-person compared with neither venue.4 Another study found increased odds of both CT and NG among individuals who met sex partners on geosocial networking applications compared with individuals who met in-person only.5
In March 2020, the State of California issued an executive shelter-in-place order (COVID-19 lockdown) to help prevent SARS-CoV-2 transmission; however, the COVID-19 pandemic may have had negative consequences for sexual health in the USA.2 6 For example, pandemic-response efforts caused many healthcare clinics to close or limit in-person visits, thereby reducing screening and testing for asymptomatic STIs.2 At the same time, social distancing measures may have decreased in-person interactions, offsetting the need for STI screening during the pandemic.2 7
Currently, the relationships between NG and CT infections and venues where MSM met sex partners amid COVID-19 pandemic shelter-in-place orders are understudied. Moreover, the relationship between NG and CT infection and where MSM meet sex partners (such as meeting in-person vs online) is understudied, with no studies assessing the impact of COVID-19 on this relationship.
The COVID-19 pandemic further raised concerns about where MSM meet sex partners, since shelter-in-place orders limited the ability to meet sex partners at in-person venues due to closures of these spaces.6 8 At the beginning of the COVID-19 pandemic, many MSM increased their use of dating applications to connect with other men online; however, this did not directly translate to an increase in meeting sexual partners through online methods.9 10 Within 1 month of the initial shelter-in-place order, MSM did not change the frequency of using dating apps to meet people in person.10 However, there is a gap in research as to whether this changed as shelter-in-place orders were extended while the pandemic progressed. As such, with community venues being closed or operating at reduced capacity for an extended period due to the COVID-19 pandemic, it is plausible that MSM shifted to meeting sexual partners online as the pandemic progressed.
This study had three objectives. The first objective was to describe changes in demographics and STI-associated behaviours, the prevalence of CT/NG and the venues where MSM meet sex partners before and during the COVID-19 pandemic. The second objective was to investigate the association between venues where MSM meet sex partners and CT/NG prevalence before and during the COVID-19 pandemic, while controlling for demographics that significantly differed between time periods. Lastly, the third objective was to determine whether any factors significantly modified the relationship between venue and STI status, using a parsimonious fit model.
Methods
Study design and sample
We used data from adult participants who received STI testing at the ‘Good To Go’ (GTG) sexual health clinic in San Diego, California during two time periods: (1) pre-COVID-19 (March–September 2019) and (2) during COVID-19 (March–September 2021). The GTG clinic provided free, community-based, confidential acute and early HIV infection and STI screenings. To receive testing at the GTG clinic, participants were required to be ≥18 years old, report one or more behaviour that could increase risk of acquiring HIV during the previous 6 months and report HIV-negative or unknown HIV status. GTG primarily targeted MSM and transgender individuals with risk of HIV infection, however, any person meeting the criteria could receive testing. The GTG screening process included HIV testing for acute and established infection,11–13 reverse sequence algorithm syphilis testing14 and self-collection of three-site samples for CT and NG15 (urine, posterior pharynx and rectal). Participants were offered testing from all three anatomical sites but had the option to decline one or more tests. If a test produced an invalid result, the test was repeated on the original sample. A self-administered survey was administered to collect demographic and behavioural information.
Measures
STI outcome measure
CT and NG infections were detected using the Cepheid GeneXpert (Sunnyvale, California, USA) CT/NG Rapid PCR from urine, oropharynx and rectal samples.16 The Cepheid CT/NG Xpert Test is a validated, Nucleic Acid Amplification Test (NAAT)-based point-of-care, test to detect bacterial STIs in urogenital samples, as well as extragenital sites, such as the rectum and pharynx.17 Test results from either STI (CT or NG) and any collection site (urethral, rectal or pharyngeal) were combined into one variable to align with the study aims. Therefore, if participants tested positive for CT or NG at any collection site, they were categorised for our binary-dependent variable as having a prevalent STI.
Venue exposure measure
Participants were asked to self-report all the places where they met any sex partners in the last 3 months. We then categorised the ways that participants reported meeting sex partners in the past 3 months into three groups: (1) only met partners in in-person venues (ie, bars, clubs, gyms, outdoors, bathhouses, sex clubs, school, work, through friends/family); (2) met partners via online venues (ie, mobile apps, websites and both online and in-person) and (3) only had existing sex partners (ie, did not have new partners in the past 3 months). Participants who self-reported meeting sex partners at both in-person and online venues were categorised into the online category since previous studies have shown that meeting any sex partners online is associated with higher odds for STIs.5
Covariates
As numbers of sexual partners and recent drug use (excluding marijuana) have been associated with venues where people meet sex partners and STI outcomes,18 19 we considered these variables as possible covariates. Drug use in the past 3 months was coded to include barbiturates/tranquillisers, crack, cocaine, ecstasy, erectile disfunction medications, gamma hydroxybutyrate, heroin, ketamine, methamphetamine, nitrates/nitrites, prescription pain medications and steroids. Other measured covariates previously shown to be associated with STIs included age at enrolment, sex, gender, sexual orientation, race and ethnicity.20–22 Finally, elevated STI prevalence has been observed among some individuals using pre-exposure prophylaxis (PrEP) for HIV prevention,23 so we included PrEP use in the past 2 weeks (yes/no) as a covariate. We also controlled for year of enrolment to address potential unmeasured effects of the COVID-19 pandemic.
Statistical analyses
Data from participants who self-identified as male and reported having sexual intercourse with other males in the 3 months prior to their visit were included in the analysis. We calculated descriptive statistics for the study sample overall and stratified by enrolment period. Welch’s t-test, χ2 test and Wilcoxon rank-sum test assessed whether sociodemographics (age, race, ethnicity, sex at birth, gender identity, sexual orientation) and sexual behaviours (number of sex partners in the past 3 months, PrEP use in the past 2 weeks, drug use in the past 3 months) differed between participants recruited before versus during COVID-19.
Multivariable logistic regression identified associations between venues where MSM met sex partners and CT/NG prevalence. The reference group for venue was only having sex with existing partners in the past 3 months. We adjusted for enrolment period and covariates (age, race, ethnicity, number of sex partners, drug use and PrEP use). Additional analyses examined whether year, number of sex partners or age acted as effect modifiers of associations between venues and prevalent CT/NG, including determining a parsimonious fit model. The interaction between venue and number of sex partners was included in the final multivariable logistic regression due to a statistically significant parsimonious fit. All analyses were performed using R V.4.0.2.24
Results
Sample characteristics
Among 2546 participants, 59.0% were under the age of 35 (range: 18–79) years, 27.9% were non-white and 37.0% were Hispanic/Latino (table 1). In the past 2 weeks, 18.2% had used PrEP. In the past 3 months, 15.3% reported drug use, and the median number of unique sex partners was 3 (IQR 2, 5). The two groups differed by age, race, ethnicity, sexual orientation, use of PrEP and number of sex partners (all p<0.05).
Compared with those who enrolled pre-COVID-19 (n=1554), in the past 3 months, more participants who enrolled during the COVID-19 pandemic (n=992) had only existing sex partners (22.0% vs 32.9%) and fewer met sex partners online (58.9% vs 53.7%) and in in-person venues (19.1% vs 13.4%) (table 1).
STI prevalence
Of the participants who received CT/NG testing, 78.5%, 94.3% and 94.0% provided rectal, pharyngeal and urine samples, respectively. The prevalence of STIs was highest in extragenital samples (table 2). The prevalence of STIs was higher among participants enrolled during COVID-19 compared with pre-COVID-19 for all collection sites, except for pharyngeal CT (table 2). There was an increase in the prevalence of STIs among participants recruited during COVID-19 compared with those recruited pre-COVID-19 (13.3% vs 17.0%, p=0.01).
STI prevalence by venues for meeting sex partners
STI prevalence was higher among participants who enrolled during compared with pre-COVID-19 for each venue category (figure 1). In 2019, the prevalence of STIs for in-person venues was similar to the prevalence for existing partners; however, in 2021, the prevalence for in-person venues increased significantly to nearly the same prevalence as online venues.
Multivariable logistic regression
Using multivariable logistic regression analysis, we found that compared with having only existing sex partners in the past 3 months, meeting new sex partners online was associated with higher odds of prevalent STIs (adjusted OR (aOR) 2.32; 95% CI 1.51 to 3.65) (table 3) while meeting new sex partners in-person was not associated with prevalent STIs (aOR 1.59; 95% CI 0.87 to 2.89). Furthermore, the odds of having prevalent STIs were higher among those enrolled during versus pre-COVID-19 (aOR 1.42; 95% CI 1.13 to 1.79). Age, number of sex partners and PrEP use were also significantly associated with prevalent STIs, whereas race, ethnicity and drug use were not (table 3).
Effect modification
We also investigated effect modification on the associations between venue and prevalent STIs by enrolment year, age, drug use and number of sex partners. Each model with an interaction term was checked for parsimonious fit using analysis of variance likelihood ratio tests. The models for venue and STI status which included year of enrolment, age and drug use were not the best fitting models; however, the model which included the interaction by number of sex partners accomplished the most parsimonious fit (p=0.001). Among participants who met sex partners in-person, the odds of STIs increased by 8.58% per 1-unit increase in the number of sex partners. Among participants who met sex partners online, the odds of STIs increased by 2.63% per 1-unit increase in the number of sex partners.
Discussion
In this large sample of MSM presenting at a sexual health clinic before and during the COVID-19 pandemic, we identified independent associations between the venues where participants met new sex partners and enrolment period (pre-COVID-19 and during COVID-19) with CT/NG. Of note, we observed a significant increase in STI prevalence for MSM who met sex partners in-person between enrolment periods. The prevalence of STIs for this group was similar to those with only existing sex partners pre-COVID-19, but shifted during COVID-19 to be more similar to online venues. At the same time, we noted an increase in the proportion of MSM who only had existing sex partners during COVID-19 compared with pre-COVID-19, which could demonstrate an attempt to decrease the risk of COVID-19 transmission (eg, by only having sex with known, trusted partners while avoiding strangers or anonymous partners) or fewer opportunities to meet partners in-person due to physical distancing guidelines or shelter-in-place orders. Regardless, over 50% of participants reported using online methods to meet sex partners in both enrolment periods, highlighting a continued need to educate mobile application users about STI transmission and local testing and treatment resources.25
Compared with only having existing sex partners, there was an increased odds of STIs among participants who met partners online, which is consistent with other literature showing this association.4 5 The prevalence of STIs among participants during COVID-19 was also higher than the pre-COVID-19 period. However, our study did not find that the association between STI prevalence and venue changed across time intervals. This is consistent with research conducted early in the pandemic showing that MSM were increasingly connecting with others online but that these connections were not leading to increased sexual encounters.9 10
We also found that, while the prevalence of STIs increased between time periods, the number of sex partners declined. One potential reason for the increase in STI prevalence during COVID-19 could be barriers to clinical care, including a reduction of testing and treating STI infections during the pandemic. One recent prospective cohort study based in Baltimore, Maryland found that STI testing significantly decreased during the beginning of the pandemic, but was restored to pre-COVID-19 levels by the end of 2020.26 Of note, this particular study found no change in prevalence of CT and NG, however, the researchers provided at-home test kits to their participants, thus being unable to account for the impact of clinical closures on this relationship.26 Although the State of California recently passed legislation allowing state-regulated private insurance plans to reimburse at-home STI collection kits,27 further research is needed that focuses on reducing barriers to STI testing such as clinical closures, privacy, stigma and cost.
It is important to note that those who met sex partners at in-person venues had the largest increase in the prevalence of STIs between enrolment periods. Furthermore, the odds of prevalent STIs associated with increasing numbers of sex partners was greater among participants who met new sex partners at in-person venues compared with online venues. This could indicate that MSM who met sex partners in-person during the pandemic were also more likely to exhibit behaviours that may increase the risk of STIs than those who were maintaining social distancing measures throughout the pandemic.
Limitations and strengths
There were specific limitations to this study. Notably, due to the cross-sectional design, we cannot determine causality or temporality between the identified associations. Furthermore, we used two cross-sectional samples from different time periods; as such, the differences we observed could relate to differing samples rather than actual behavioural changes over time. Similar to other studies based on sexual health clinic populations, our findings might overestimate STI prevalence among MSM overall because participants seek testing and treatment due to possible exposure or symptoms.28 One limitation with categorisation was including public sex environments (PSE) and commercial sex venues (CSV) into the in-person category, even though sexual behaviours can vary between private locations, PSE and CSV. For example, those who have sexual encounters in a CSV are more likely to have multiple sex partners and sex with anonymous partners.29 However, few MSM reported meeting through PSE and CSV. We also categorised MSM who met sex partners both online and in-person into the online category, which did not separately account for those who use multiple modalities for meeting sex partners. This overlap in categorisation could skew data, as it is possible that individuals who use multiple modalities to meet sex partners could have different risks for STIs. Therefore, future studies should further disaggregate the venues where MSM meet sex partners to determine whether these significant differences remain true when held in separate categories. Furthermore, alcohol and marijuana were not evaluated for this study, however, could be possible covariates for this analysis. Our study also had several strengths. Given the study period overlapped with the start of the COVID-19 pandemic, we were able to examine STI prevalence during the COVID-19 pandemic among MSM. Furthermore, STI results were based on NAAT at a clinic using samples from three anatomic sites, thus providing objective and comprehensive STI prevalence estimates.
Conclusion
We hypothesised that due to the closure of in-person venues during the COVID-19 pandemic, MSM would be more likely to meet sex partners through online methods. Our study did not identify a significant interaction between venues and enrolment year, demonstrating that changes in STI prevalence did not result from the increased use of online venues during the pandemic. However, we found that meeting sex partners online was associated with increased CT/NG prevalence among participants of a sexual health clinic during this time period. Furthermore, we found that the prevalence of STIs appeared to increase during the COVID-19 pandemic compared with pre-COVID-19.
Future studies should continue to assess the impact of the COVID-19 pandemic on the relationship between venues where MSM meet sex partners and STI transmission, as this relationship could change as the pandemic evolves. Collecting data in future studies that specifically assesses the use of online apps while at in-person venues will be necessary to further assess the intersection of this relationship. Qualitative studies could also help elucidate barriers to STI testing and treatment, protective measures and possible strategies that could support access to STI testing and treatment. While online venues provide an avenue for STI prevention education, these programmes can be expensive. Additional support (including insurance coverage) for at-home STI testing could help reduce barriers to access. Since STI rates are expected to continue increasing post-COVID-19 pandemic, interventions are needed to address these barriers long-term.30
Data availability statement
Data are available on reasonable request. De-identified participant data are available through the UC San Diego Antiviral Research Center (UCSD AVRC) by emailing the database administrator, Tara Tenenbaum, at tchaloukian@ucsd.edu.
Ethics statements
Patient consent for publication
Ethics approval
The University of California, San Diego Institutional Review Board reviewed and approved this study protocol (#180747). Participants gave informed consent to participate in the study before taking part.
Acknowledgments
We gratefully thank the participants of the Primary Infection Resource Consortium.
References
Footnotes
Handling editor Jamie Scott Frankis
Twitter @the_colin_king
Contributors CMBK conducted the data analysis, wrote the manuscript, and is the guarantor of this publication. BS, RSG, ARB, SJL made editorial contributions and provided direction for the manuscript and analysis. BS and SJL coordinated the data collection. All individuals made significant contributions to this work to qualify for authorship.
Funding This work was supported by National Institutes of Health grants (AI106039, MH100974, K01DA049665 and K01DA043412) and the James B. Pendleton Charitable Trust. My coauthors have read and approved the final manuscript.
Competing interests SJL has received funding from Gilead Sciences paid to her institution and donation of medications from Gilead Sciences.
Provenance and peer review Not commissioned; externally peer reviewed.