On March 4th, 2020, a state of emergency was declared in California in response to the COVID-19 pandemic, beginning what would become a multi-year cycle of tightening, loosening, and modifying policies aimed at reducing the burden of COVID-19 [1]. Through these policies, as well as individual concern of becoming infected with the novel virus, the pandemic significantly impacted healthcare by limiting in-person healthcare visits, redirecting resources to COVID-19 related efforts, and contributing to a rise in healthcare worker burnout and attrition [2–4]. The pandemic also affected access for sexual health services, including services for sexually transmitted infections (STIs) [5].

Although a significant number of STIs are asymptomatic in nature, guidelines to test and treat only those experiencing symptoms were encouraged [6]. Additionally, policies that were enacted to curb a COVID-19 surge diverted resources from STI and HIV screening and treatment centers [7]. For example, a retrospective study among an open cohort of Kaiser Permanente of Southern California members found substantial decreases in testing and diagnoses of STIs during the COVID-19 pandemic compared to the three years prior, likely explained by reductions in asymptomatic screening [8]. Furthermore, some healthcare facilities became less available. For example, centers such as the Berkeley Free Clinic in Berkeley, California, which offers free STI screening and treatment, closed for remote and in-person services for a significant period [9]. With many healthcare centers resorting to online video visits, those without access to privacy, stable internet connection, adequate technology, or the ability to access and return samples, were unlikely to receive necessary testing [10, 11]. These policies likely impacted STI treatment access and the forward transmission of STIs, which may have accelerated with less treatment engagement.

Men who have Sex with Men (MSM) are a population that is disproportionately affected by STIs, which could cause direct health impacts or increase the risk for HIV infection [12, 13]. However, little is known about how STI risk, or the risk of acquiring STIs through sexual behaviors with multiple partners, with suboptimal levels of barrier or biomedical protection, or through event-driven substance use that affects adherence to protection, changed for MSM, if at all, during the COVID-19 pandemic [14]. Prior to the pandemic, STI rates were on the uptrend in the United States. Syphilis infection cases among MSM increased 11.2%, from 16,155 to 17,968 between the years of 2016 and 2020 [15]. At the start of the COVID-19 pandemic, between March through April 2020, STI rates decreased likely due to a combination of fewer people being screened and fewer interactions between MSM, but rates began to increase again by the end of the year [16–18]. San Francisco, saw a similar pattern unfold. According to the San Francisco Department of Health there was a 34% increase in syphilis, 16% increase in gonorrhea, and 12% increase in chlamydia between 2016 and 2019, but a 17% decrease in syphilis, 39% decrease in chlamydia, and 26% decrease in gonorrhea between 2019 and 2020 [19]. There was also a sharp decrease in STI screening rates at the start of March 2020, which were still at pre-pandemic levels over a year later in August 2021, indicating that the decreases seen in San Francisco could in part be explained by insufficient screening [19]. Despite what should have been an apparent drop in STI rates, the Centers for Disease Control (CDC) reported that incidence among MSM increased, disproportionately affecting minority communities, the reasons for which, are multifaceted, complex, but not fully elucidated [20].

For MSM, COVID-19 has affected healthcare through a reduction in access to services such as HIV and STI testing, HIV care needs, and access to other services, which could have led to missed diagnoses and a higher risk for onward transmission [21, 22]. Sexual networks were also altered, with a study in San Francisco finding that some MSM became abstinent during this period, while others had no changes or even reported increases in the number of sexual partners [23]. Some of the practices employed to reduce COVID-19 risk included being part of small social circles, which were endorsed by some local governments; however, how these attempts to mitigate the acquisition of a respiratory infection affected STI risk is not well understood [24]. Furthermore, prolonged COVID-19 shelter-in-place policies increased mental distress and substance use during the COVID-19 pandemic, which in turn may have increased STI risk [25–28]. Untangling the impact of factors affecting STI risk among MSM during the COVID-19 pandemic may help inform the development of interventions to reduce STIs among MSM. Moreover, identifying MSM at risk for STIs can help inform targeting of novel biomedical interventions, including doxycycline post-exposure prophylaxis (DoxyPEP), which may reduce the need for in-person clinic visits and has demonstrated efficacy in reducing bacterial STIs [29].

The Socio-Ecological Model (SEM) is a framework that is designed to examine how multilevel factors affect the health and behaviors of individuals [30]. It posits that motivations are influenced not just by internal drivers or perceptions, which are mediated by factors such as mental health, substance use, or personal belief systems, but by the context of an individual’s surroundings, such as policies, culture, economic situation, access to healthcare, as well as the nature of interpersonal relationships. In regards STI risk among MSM, the SEM model is a useful framework to examine how risk-taking behaviors unfold to explain the higher rates of STIs among this population [31, 32]. Further, the SEM model can pinpoint areas to intervene at any of these levels which may have salient implications for STI risk mitigation. To reduce these gaps in research, we assessed and analyzed data capturing behaviors of MSM during the peak of the COVID-19 pandemic to examine COVID-related structural, interpersonal, and individual risk and/or protective factors for STI risk during this period [30]. Findings from this study may help inform policies to reduce STIs among MSM in the context of a pandemic.

This study utilized secondary data from the MSM cycle of the National HIV Behavioral Surveillance (NHBS) study in San Francisco, conducted from June 2021 through December 2021. NHBS is a CDC led collaboration of health jurisdictions across the US which samples MSM, as well as people who inject drugs and high-risk heterosexuals on a 3-year cycle [33]. NHBS historically utilized time location sampling at physical venues to obtain relatively large quasi-probability samples of MSM. However, in response to the COVID-19 pandemic, study recruitment was conducted by intercepting potential participants in virtual venues such as dating apps and through advertisements on social media sites targeting persons with interests in LGBT topics. The use of online venues for sampling MSM was intended to be analogous to the use of physical venue for the usual cycles of NHBS for MSM. A pre-survey formative research phase was conducted using in-depth interviews with community stakeholders and leaders to gather information on popular dating apps and social media sites used by MSM in San Francisco. Based on findings from this formative phase, the study identified a comprehensive list of apps used by MSM. Randomly selected app-day time slots were used to conduct recruitment activities. Potential participants were sent a brief introductory message to assess their interest in participating in this study. Interested participants called the study phone line to be assessed for eligibility based on the following inclusion criteria: being 18 years or older, identifying as a cisgender man, reporting a male sexual partner in their lifetime, and residing in San Francisco, California. Eligible participants scheduled an online study visit, provided verbal consent, and completed the virtual interviewer-administered survey on zoom or through phone call. The participants were offered the opportunity to be tested for HIV using an at-home OraQuick HIV testing kit, which were mailed to the participants. HIV test results and STI specimens were either mailed back to the study site or dropped in person.

Participants were asked about their demographic information, such as age in years, race/ethnicity, highest level of education, and access to healthcare in the past 12 months. Most questions referenced the previous 12-month period, or June 2020–Dec 2020, at a time when healthcare systems were still impacted by the pandemic and shelter-in-place ordinances were still in place to mitigate COVID-19 risk. In addition, participants were asked about sexual and substance use risk behaviors, such as “Within the past 12 months, how many sexual partners have you had?”; and “How often have you used (substance class) in the past 12 months?” The substance classes evaluated included methamphetamine, powdered cocaine, painkillers, heroin, ecstasy, and poppers. The PrEP questions included participants who had taken PrEP in the past 12 months (yes/no). The participants were asked to self-report their HIV status. Participants received $75 to complete the survey.

To assess STI diagnoses, participants were asked “In the past 12 months, had a doctor or other healthcare provider told you that you had [gonorrhea, chlamydia, syphilis] (yes/no)? The outcome of interest for this study was derived from this question and was any self-reported STI diagnosis in the past 12 months (yes/no), including gonorrhea, chlamydia, or syphilis. We excluded from this outcome variable any viral STIs that were asked about, including HIV, Herpes Simplex Virus, or Hepatitis C infection.

To measure exposures of interest, we were guided by the SEM (see Fig. 1) and asked participants several questions related to how the pandemic may have caused disruptions in access to care, sexual behaviors, substance use, and depression. Due to small sample sizes that could not allow for ordinal analysis, all responses were dichotomized as follows:

In our study of MSM in San Francisco during the COVID-19 pandemic, we found that structural factors related to the Covid-19 pandemic presented serious barriers to accessing sexual health services for MSM in San Francisco. Nearly one-quarter of the participants reported having had an STI infection within the previous 12-month period. The prevalence of self-reported syphilis was consistent with a similar study prior to Dec 2019, and gonorrhea and chlamydia were slightly higher in this study [37]. We found that barriers to STI testing, changes in sexual networks, and an increase or relapse in recreational substance use due to COVID-19 were independently associated with having an STI infection. Furthermore, we found that risk factors associated with STI infection prior to the COVID-19 pandemic still held in this study, including factors such as PrEP use, number of sexual partners, and the use of recreational substances, indicating that the COVID-19 pandemic did not significantly alter the behavioral risk profile of MSM in San Francisco. Risk may have been modified so that some MSM had their risk increased while it decreased for others, as nearly a quarter of MSM reported not having any sexual relationships during the social distancing period. Finally, even among those who reported no sexual behavior, STI infections were still reported, which could be explained by changes in behavior after vaccination or waning of COVID-19 cases.

MSM who encountered barriers to STI testing likely had an increased self-perceived risk of STI. That is, MSM were motivated to undergo STI testing because they engaged in sexual practices or may have experienced some of the symptoms of STIs. Without adequate testing and treatment, there is an increased risk of forward transmission of STIs and the risk of long-term sequelae of these infections, such as neurosyphilis, prostatitis, or epididymo-orchitis [38, 39]. Public health officials should not assume that STI risk will decrease during a pandemic and should prioritize making at-home test kits and treatment affordable, timely, and accessible from over the counter.

A promising new tool for the reduction of STI incidence is DoxyPEP, which can be incorporated into future pandemic planning responses that do not require in-person STI clinic visits [29]. Our findings may help identify efforts to increase uptake and expand roll-out of DoxyPEP, such as MSM who use substances and have condomless sex with multiple partners, who were observed to have increased risk of STI diagnoses.

We also found that sexual behavior was not significantly modified during the pandemic and that public health recommendations for creating small social circles were not protective against STI risk among MSM. Sexual relationships with partners whose risk for COVID was unknown and sexual relationships with people in small social circles or pods were independently associated with STI infection. The finding that sexual relationships with people whose risk for COVID-19 is unknown could represent a lack of change in risk-taking during this period as well as a reversal in behavioral changes due to fatigue induced by strictly adhering to social distancing policies. In addition, social circles and pods were regarded as important measures to reduce COVID-19 infection risk and were encouraged by public health officials [40]. Regardless of how the risk for COVID-19 was modified by this approach, STI risk was not lowered. This suggests that we need to strengthen our understanding of what constitutes safe social pods and how to strengthen their intended boundaries, such as encouraging STI testing among pod members, as they did not reduce the STI infection risk in this study.

In this study, an increase or relapse in recreational substance use among MSM was associated with STI infection. A 2020 report among the general population found that 13% of US adults reported starting or increasing substance use to cope with stress or emotions related to COVID-19, and these effects likely disproportionally affected MSM communities who were already facing a multitude of challenges specific to minorities [25, 41]. MSM in San Francisco may have used substances to cope with social isolation associated with distancing policies that were enacted or due to the stressors associated with the COVID-19 pandemic. Substance use presents its own set of problems, such as overdose risk or other direct harm; however, with reference to STI risk, previous studies have shown a strong correlation between recreational substance use and STI infection [28, 42, 43]. When STI infections are on the rise, the resurgence of substance use during a pandemic can compromise efforts to reduce STI infections and further place MSM at risk for infection. In the event of future pandemics, policies should be informed that indefinite isolation orders without any form of social or emotional support can result in fatigue and an increase in maladaptive coping strategies, including those that increase the risk of STI.

Our study has some limitations, as it is a cross-sectional study that limits our ability to determine longitudinal individual-level risk modifications by policies aimed at reducing COVID-19 infections. The representativeness of MSM in this study is also unclear, as recruitment was conducted online due to the COVID-19 pandemic. As a secondary analysis of a study of HIV risk, questions pertaining to STIs were not framed to assess risk during the height of the pandemic; therefore, there may not be a complete overlap between questions regarding disruptions due to COVID-19 and whether they were diagnosed with an STI in the past 12 months. Similarly, because no time variables were collected, we were unable to control for those periods of time that had a greater effect than others. Along these lines, the COVID-19 pandemic unfolded in unpredictable ways that could result in recall bias from participants, as some questions may have alluded to specific timepoints during the pandemic that were more memorable than others. The sample includes only people using the Internet to find MSM partners and is self-selected in ways that cannot be controlled. Thus, our results may not be generalizable to the MSM population in San Francisco or to MSM in other cities. This is especially pertinent to the fact that over 75% of the sample was older than 32 years, which is not catching the younger age groups that are typically more at risk for STI infections. Additionally, the outcome of STI diagnosis was based on self-reported results (i.e. the study did not conduct STI screening). Moreover, data collection occurred during a period when STI screening services were likely impacted. Hence, misclassification bias may have occurred and it’s likely that those with asymptomatic STIs were not captured in this outcome measure. Therefore, our findings should be interpreted with caution, with these limitations in mind.

Despite these limitations, this study indicates that multiple structural, interpersonal, and individual factors because of the COVID-19 pandemic was associated with increased STI risk. Based on our findings, we recommend that future pandemic mitigation strategies balance efforts to minimize these multi-level disruptions in sexual health services for MSM and which can help to reduce STIs. These findings suggest that, in the setting of future pandemics, public health policies could prioritize comprehensive STI prevention strategies, testing, and treatment, including strategies that can be completed remotely or at home.