Abstract
Background
The COVID-19 pandemic affected sexually transmitted infection (STI) testing and diagnosis rates in the United States (U.S.), but these patterns have not been well characterized among people with HIV (PWH).
Methods
We analyzed medical records data of HIV Outpatient Study (HOPS) participants seen for HIV care from January 2019—March 2021, with ≥1 CD4+ cell count and viral load test results recorded. We used Poisson regression models to estimate rate ratio (RR) and 95% confidence interval (CI) to compare STI testing and diagnoses rates on/after vs before March 1, 2020 (early COVID-19 pandemic (pandemic) vs. pre-pandemic).
Results
Of 2,311 eligible patients, STI tests (STI cases, primarily defined as tests that were positive) were as follows during the analysis timeframe: 4,991 gonorrhea (157), 4,978 chlamydia (135), and 4,216 syphilis (114). Comparing pandemic vs. pre-pandemic periods, STI testing RRs were 0.78 for both gonorrhea (CI: 0.73–0.82) and chlamydia (CI: 0.73–0.83), and 0.93 for syphilis (CI: 0.88–0.99); diagnosis rates were not statistically different. Multivariable models showed reduced testing for gonorrhea (adjusted RR 0.79, CI: 0.72–0.87) and chlamydia (adjusted RR 0.78, CI: 0.71–0.86) for men who have sex with men, but not for other HIV transmission groups.
Conclusions
The fallout of the COVID-19 pandemic on sexual health may not be seen for some time. Despite reduced STI testing, rates of STI diagnoses did not decrease. It will take a return to more routine screening and improved access to sexual health care to uncover the true impact of undetected or untreated STIs.
Keywords: HIV, gonorrhea, chlamydia, syphilis
SHORT SUMMARY
Our research explores the differences in testing and rates of STI diagnoses between COVID-19 pre-pandemic and pandemic eras in a diverse population of U.S. patients receiving HIV care.
Introduction
The COVID-19 pandemic caused significant HIV care continuum disruptions, largely attributed to social distancing measures1,2. Many HIV providers initiated, or substantially scaled-up telemedicine visit capacity, but these services did not completely replace the routine delivery or quality of outpatient HIV care. Tedaldi et al., examined HIV Outpatient Study (HOPS) data and found that small increases in telemedicine visits did not outweigh a larger decline (26%) in office visits. 1 Grov et al, found that among 152 people with HIV (PWH), 30.9% did not maintain an HIV-related medical appointment, and 13.8% did not retrieve HIV medications during this time2. These studies demonstrate that despite a transition to telemedicine, which occurred as a results of shutdown orders and COVID-19 mitigation strategies, PWH were not as engaged in care and had lapses in medication adherence.
Social distancing measures not only disrupted access to routine outpatient medical care, but also affected sexual behaviors and access to routine STI testing. During the pandemic, more people shifted to stay at home, presenting increased opportunities for sexual activity in the home, but simultaneously closing opportunities outside of one’s home, such as sex parties and bathhouses3–5. It is unclear how these changing sexual behaviors affected sexually transmitted infection (STI) incidence rates. Simultaneously, there were impacts on access to STI testing in the United States (U.S.). In the Spring of 2020, a national study of STI programs demonstrated that 83% of STI programs were deferring STI services, 66% reported a decrease in sexual health screening and testing, and 60% of clinics experienced reduced capacity to treat STIs6. In one survey of among gay, bisexual and other men who have sex with men (MSM) in the U.S., approximately one-third reported that the COVID-19 pandemic prevented them from accessing HIV and STI testing services, despite their continued interest in testing3.
Together, social distancing, disruptions in routine outpatient HIV care and STI programming, and changes in sexual behavior affect STI transmission and detection. This study aimed to assess differences in testing and rates of STI diagnoses between COVID-19 pre-pandemic and pandemic eras in a diverse population of U.S. patients receiving HIV care.
Materials and Methods
The HIV Outpatient Study
The HOPS is an ongoing prospective observational cohort study of adults ≥18 years diagnosed with HIV, receiving care at participating HIV clinics since 1993. The HOPS is an open cohort: patients may enter the study at any point after an HIV diagnosis and may leave the study at any point7. Patient data, including sociodemographics, diagnoses, antiretroviral therapy (ART), other treatments, and laboratory values (including CD4+ lymphocyte cell counts/mm3 [CD4] and plasma HIV RNA levels [viral load, VL]) are abstracted from medical charts and entered into a database by trained medical record abstractors. These data are reviewed for quality and analyzed centrally.
Ethics
Since its inception, the HOPS has been reviewed and approved annually by the institutional review boards of the Centers for Disease Control and Prevention (CDC) (Atlanta, GA, USA), Cerner Corporation (Kansas City, MO, USA) and each HOPS site. The study protocol conforms to the guidelines of the U.S. Department of Health and Human Services for the protection of human subjects in research. All participants provided written informed consent.
Study population
We analyzed medical record data from HOPS participants who received HIV care at eight U.S. HIV clinics (university-based, public, and private) in six U.S. cities (Chicago, IL; Denver, CO; Stony Brook, NY; Philadelphia, PA; Tampa, FL; and Washington DC) during the analysis timeframe: 1/1/2019 to 3/31/2021 using the HOPS dataset cumulative through 9/30/2023. Participants had to have at least one visit, and at least one CD4, and one VL test result during the analytic time period of 1/1/2019 to 3/31/2021 to be included in analysis. The first HOPS encounter during the analytic period is considered the baseline date. For those who ended the HOPS study prior to 3/31/2021, observation ended on their last encounter date.
Measurements and definitions
Baseline demographic variables included age group (18–30, 31–40, 41–50 and ≥ 51 years); sex at birth; race/ethnicity (non-Hispanic/Latino Black, non-Hispanic/Latino White, Hispanic/Latino or other/unknown race/ethnicity); HIV transmission risk (ordered hierarchically using the following priority: people who inject drugs [PWID], MSM, heterosexual males and females, and other/unknown HIV risk); insurance (private, public or none); clinic type (public or private); HOPS entry year (before 2019, and 2019–2021); CD4 count (< 200, 200–349, 350–499 and ≥500 cells/mm3); VL (< 200 and ≥ 200 copies/mL); presence of an AIDS diagnosis; ART history (experienced, naïve, or unknown); and current or prior smoking status (yes, no). If a VL test result was undetectable, the VL quantity was assigned a value of half the lower limit of test detection for analysis. We defined gonorrhea (GC) or chlamydia (CT) diagnosis based on evidence of either a positive laboratory result or a clinical diagnosis recorded on a patient’s medical chart; To avoid test overcount, when multiple GC or CT tests were conducted on different anatomic sites on the same day and same patient, we only counted it as one test, and referred it as one test per patient-test date. When there were multiple positive anatomic sites within one patient-test date, we only counted it as one positive test result. We defined syphilis diagnosis based on the evidence of any of the following: a 4-fold increase in rapid plasma regain (RPR) titer, a positive qualitative syphilis screen with a prior negative result, or both a documented syphilis diagnosis and record of treatment for syphilis. In addition, if a participant’s first recorded syphilis test result was positive, and there was no prior test history, but there was corroborative concurrent syphilis diagnosis or treatment evidence, then the participant was considered to have syphilis. Outcomes of interest were the testing and diagnosis of GC, CT or syphilis during the analytic time period. Within that timeframe, we specified two periods: 1/1/2019–2/29/2020 (pre-COVID-19 pandemic era) and 3/1/2020–3/31/2021 (pandemic era) to help capture immediate effects of stay-at-home mandates on STI testing and incidence. Participants did not have to have visits during both (pre- and pandemic) time periods.
Statistical analyses
We calculated GC, CT and syphilis testing and diagnosis rates overall, and by pre-pandemic versus pandemic period. Likelihood ratio chi-square or Fisher exact tests (utilized when at least 25% of cells had expected counts less than five) were used to compare patient characteristics (binary or categorical variables) and Kruskal-Wallis or Wilcoxon rank-sum tests were used to compare continuous variables by outcome (testing or cases yes/no). Associations of GC, CT and syphilis testing and diagnosis rates were estimated, and rate ratios (RRs) were compared between pre-pandemic and pandemic periods. For this we used univariable Poisson regression stratified by sociodemographic and clinical factors. These models accounted for repeated observations on individuals during observation using a random intercept term for our models. To derive adjusted rates and rate ratios (aRRs), we constructed multivariable models by backwards elimination. Initially, all factors were included as main effects along with time period (pre-pandemic or pandemic) and all interactions for each factor with time period. Factors were then removed one-at-a-time with ‘stay’ criteria set to P<0.05 (factors that had interaction terms with time period with P<0.05 remained as main effects regardless of their main effect P-value). From the final multivariable models, linear contrasts of appropriate resulting parameters were used to estimate aRRs for various stratum-specific comparisons of pre- vs. pandemic periods simultaneously adjusted for other factors. Results with P<0.05 were considered statistically significant. All Poisson models included a person-time offset.
OpenEpi version 3.01 (Emory University, Atlanta GA http://openepi.com/Menu/OE_Menu.htm) was used to calculate 95% confidence intervals (CIs) around testing and diagnosis rates, assuming a Poisson distribution. Descriptive summaries of data, and univariable and multivariable Poisson regression were done using SAS version 9.4 (SAS Institute, Cary, NC).
Results
Among 10,886 HOPS participants who consented to participate as of 9/30/2021, 2,316 had at least one encounter during the 1/1/2019–3/31/2021 analysis timeframe; 2,311 had at least one CD4 and VL test recorded during observation (Table 1).
Table 1:
Demographics and clinical characteristics of study sample from the HIV Outpatient Study, 1/2019–3/2021 (n=2,311).
| Characteristics at first visit during observation | Overall 1/2019–3/2021 n (%) | Contact* during 1/2019–2/2020 n (%) | Years of observation: 1/2019–2/2020 | Contact during 3/2020–3/2021 n (%) | Years of observation: 3/2020–3/2021 |
|---|---|---|---|---|---|
| Overall | 2,311 (100.0) | 2,257 (100.0) | 2,410.8 | 1,994 (100.0) | 1,700.5 |
|
| |||||
| Age, years | |||||
| <30 | 230 (10.0) | 212 (9.4) | 205.6 | 201 (10.1) | 166.2 |
| 31–40 | 393 (17.0) | 379 (16.8) | 394.3 | 331 (16.6) | 268.1 |
| 41–50 | 467 (20.2) | 459 (20.3) | 492.2 | 391 (19.6) | 325.5 |
| ≥51 | 1,221 (52.8) | 1,207 (53.5) | 1,318.8 | 1,071 (53.7) | 940.8 |
|
| |||||
| Sex | |||||
| Male | 1,758 (76.1) | 1,712 (75.9) | 1,816.7 | 1,501 (75.3) | 1,282.6 |
| Female | 553 (23.9) | 545 (24.1) | 594.0 | 493 (24.7) | 417.9 |
|
| |||||
| Race/ethnicity | |||||
| Non-Hispanic/Latino white | 933 (40.4) | 913 (40.5)* | 986.3 | 823 (41.3) | 719.4 |
| Non-Hispanic/Latino Black | 895 (38.7) | 873 (38.7) | 920.6 | 748 (37.5) | 615.3 |
| Hispanic/Latino | 398 (17.2) | 388 (17.2) | 415.4 | 355 (17.8) | 310.9 |
| Other race/ethnicity | 85 (3.7) | 83 (3.7) | 88.5 | 68 (3.4) | 54.9 |
|
| |||||
| HIV transmission risk group | |||||
| PWID | 152 (6.6) | 149 (6.6) | 157.5 | 132 (6.6) | 113.4 |
| MSM | 1,283 (55.5) | 1,251 (55.4) | 1,334.3 | 1,102 (55.3) | 945.5 |
| Heterosexual male | 276 (11.9) | 268 (11.9) | 280.8 | 240 (12.0) | 208.0 |
| Female | 457 (19.8) | 450 (19.9) | 488.9 | 406 (20.4) | 349.0 |
| Other risk | 143 (6.2) | 139 (6.2) | 149.3 | 114 (5.7) | 84.6 |
|
| |||||
| Insurance payor | |||||
| Private | 1,056 (45.7) | 1,035 (45.9)* | 1,118.8 | 922 (46.2) | 786.5 |
| Public | 1,194 (51.7) | 1,162 (51.5) | 1,232.0 | 1,026 (51.5) | 878.5 |
| Other/unknown/none | 61 (2.6) | 60 (2.7) | 59.9 | 46 (2.3) | 35.5 |
|
| |||||
| Clinic type | |||||
| Public | 1,251 (54.1) | 1,218 (54.0) | 1,286.8 | 1,081 (54.2) | 924.0 |
| Private | 1,060 (45.9) | 1,039 (46.0) | 1,124.0 | 913 (45.8) | 776.5 |
|
| |||||
| Year of HOPS entry | |||||
| Before 2019 | 2,093 (90.6) | 2,076 (92.0) | 2,277.9 | 1,790 (89.8) | 1,538.2 |
| 2019–2021 | 218 (9.4) | 181 (8.0) | 132.9 | 204 (10.2) | 162.3 |
|
| |||||
| CD4+ cell count (cells/mm3) | |||||
| < 200 | 155 (6.7) | 144 (6.4) | 140.3 | 123 (6.2) | 100.2 |
| 200–349 | 204 (8.8) | 199 (8.8) | 211.0 | 174 (8.7) | 149.1 |
| 350–499 | 311 (13.5) | 300 (13.3) | 313.7 | 263 (13.2) | 221.8 |
| ≥ 500 | 1,641 (71.0) | 1,614 (71.5) | 1,745.8 | 1,434 (71.9) | 1,229.4 |
|
| |||||
| Viral load (copies/mL) | |||||
| < 200 | 2,070 (89.6) | 2,042 (90.5) | 2,217.9 | 1,797 (90.1) | 1,541.5 |
| ≥ 200 | 241 (10.4) | 215 (9.5) | 192.9 | 197 (9.9) | 159.0 |
|
| |||||
| Prior AIDS diagnosis | |||||
| Yes | 1,209 (52.3) | 1,199 (53.1) | 1,303.9 | 1,026 (51.5) | 883.6 |
| No | 1,102 (47.7) | 1,058 (46.9) | 1,106.9 | 968 (48.5) | 816.9 |
|
| |||||
| Antiretroviral experience | |||||
| Experienced | 2,200 (95.2) | 2,170 (96.1) | 2,347.1 | 1,890 (94.8) | 1,619.9 |
| Naïve | 105 (4.5) | 81 (3.6) | 56.7 | 98 (4.9) | 74.7 |
| Unknown | 6 (0.3) | 6 (0.3) | 7.0 | 6 (0.3) | 5.9 |
|
| |||||
| Current/prior smoker | |||||
| Yes | 1,089 (47.1) | 1,061 (47.0) | 1128.6 | 929 (46.6) | 793.6 |
| No | 1,222 (52.9) | 1,196 (53.0) | 1282.2 | 1,065 (53.4) | 906.9 |
|
| |||||
| Received GC test during observation | |||||
| Yes | 1,397 (60.5) | 1,362 (60.3) | 1,493.1 | 1,271 (63.7) | 1,109.1 |
| No | 914 (39.5) | 895 (39.7) | 917.7 | 723 (36.3) | 591.4 |
|
| |||||
| Received GC diagnosis during observation | |||||
| Yes | 157 (6.8) | 152 (6.7) | 157.4 | 142 (7.1) | 123.5 |
| No | 2,154 (93.2) | 2,105 (93.3) | 2,253.3 | 1,852 (92.9) | 1,577.0 |
|
| |||||
| Received CT test during observation | |||||
| Yes | 1,397 (60.5) | 1,362 (60.3) | 1,493.3 | 1,271 (63.7) | 1,108.4 |
| No | 914 (39.5) | 895 (39.7) | 917.5 | 723 (36.3) | 592.1 |
|
| |||||
| Received CT diagnosis observation | |||||
| Yes | 135 (5.8) | 130 (5.8) | 138.6 | 125 (6.3) | 111.2 |
| No | 2,176 (94.2) | 2,127 (94.2) | 2,272.1 | 1,869 (93.7) | 1,589.2 |
|
| |||||
| Received syphilis test during observation | |||||
| Yes | 1,547 (66.9) | 1,509 (66.9) | 1,655.4 | 1,414 (70.9) | 1,231.8 |
| No | 764 (33.1) | 748 (33.1) | 755.4 | 580 (29.1) | 468.7 |
|
| |||||
| Received syphilis diagnosis during observation | |||||
| Yes | 114 (4.9) | 70 (3.1) | 125.6 | 50 (2.5) | 95.8 |
| No | 2,197 (95.1) | 2,187 (96.9) | 3,980.3 | 1,944 (97.5) | 3,807.9 |
Abbreviations: CT, chlamydia; GC gonorrhea, MSM, men who have sex with men, PWID, persons who inject drugs
Contact was considered to be an office, laboratory or hospital visit, or telephone/telemedicine encounter.
Sum of percentages is >100.0% due to rounding error.
Overall, most participants were: over 50 years of age (53%), male (76%), non-Hispanic White (40%), MSM (56%), publicly insured (52%), seen in a public clinic (54%), ARV experienced (95%), not current or prior smokers (53%). Additionally, most entered HOPS before 2019 (91%), had baseline CD4+ cell count of at least 500 cells/mm3 (71%), and had a VL test result of < 200 copies/mL (90%). These demographics were similar between the pre- and early-pandemic observational periods. Of the 2,311 participants, 2,257 were seen during the pre-pandemic, and 1,994 were seen during the pandemic periods. Of the 1,994, 204 (10%) had first HOPS visit during the pre-pandemic period; 54 (3%) had first HOPS visit during the pandemic period.
Gonorrhea
There were 157 GC cases among 2,311 participants and 4,991 GC tests completed during the study period (88% had a test in both pre-pandemic and pandemic eras). The majority of GC diagnoses (92%) were supported by positive laboratory result documented in HOPS medical record. The median number of GC tests per participant during the pre-pandemic period was 2 (interquartile range (IQR) 1–3), while the median tests during the pandemic period was 1 (IQR 1–3). During the pre-COVID-19 pandemic era, 90 participants had one, 15 had two, and 5 had three or more documented GC infections. During the pandemic era, 61 participants had one, 7 had two, and 5 had three or more documented GC infections. Overall, the RRs for GC test and GC diagnosis comparing the pandemic vs. pre-pandemic periods were 0.78 (CI: 0.73–0.82), and 0.99 (CI: 0.76–1.28), respectively, indicating GC testing had fallen but GC diagnosis rate had not (Figure 1). In univariable analyses, GC test rates were lower comparing pandemic vs. pre-pandemic periods for nearly all participant subgroups; in multivariable analyses, the pandemic-related testing reduction was observed for MSM (RR 0.79, CI: 0.72–0.87), those seen in a public clinic (RR 0.86, CI: 0.76–0.98) and those entering HOPS during 2019–2021 (RR 0.82, CI: 0.67–0.99) (Supplemental Table 1a). In univariable analyses, the pandemic period had a nearly seven-fold increased rate of diagnosis compared with the pre-pandemic period for those having other/unknown/no insurance (RR 6.75, CI: 2.14–29.84) and those having CD4 <200 cells/mm3 the rate during the pandemic was nearly five-fold higher (RR 4.90, CI: 1.09–34.42). In multivariable analyses, this increased pandemic period rate persisted only for those having other/unknown/no insurance (aRR 5.17, CI: 1.45–18.35) (Supplemental Table 1b).
Figure 1: (A) STI testing rates and (B) rates of STI diagnoses with 95% confidence interval bars, by COVID-19 pre-pandemic and pandemic periods, the HIV Outpatient Study, January 2019-March 2021, n = 2,311.
Abbreviations: CT, chlamydia; GC gonorrhea; STI, sexually transmitted infection.
Note: total diagnoses: GC=157, CT=135, syphilis=114.
Chlamydia
There were 135 CT cases among 2,311 participants and 4,978 CT tests completed during the study period. Similarly, the majority of CT diagnoses (92%) were supported by positive laboratory result documented in the medical record. The median number of CT tests per participant during the pre-pandemic period was 2 (interquartile range (IQR) 1–3), while the median tests during the pandemic period was 1 (IQR 1–3). During the pre-COVID-19 pandemic era, 77 participants had one, 12 had two, and 5 had three or more documented CT infections. During the pandemic era, 49 participants had one, 8 had two, and 2 had three or more documented CT infections. Overall, the RRs for CT test and CT diagnosis comparing the pandemic vs. pre-pandemic periods were 0.78 (95% CI: 0.73–0.83), and 0.84 (95% CI: 0.61–1.14), respectively (Figure 1). In univariable analyses, CT test rates were lower comparing pandemic vs. pre-pandemic periods for almost all participant demographic and clinical subgroups. In multivariable analyses, the pandemic-related testing reduction was observed for MSM (RR 0.78, CI: 0.71–0.86) and for those seen in public clinics (RR 0.85, CI: 0.74–0.96) (Supplemental Table 2a). In univariable analyses, the pandemic-period had lower diagnosis rates (compared to pre-pandemic) among those that entered HOPS before 2019 (RR 0.62, CI: 0.43–0.88), similarly those being ART experienced had lower rates of CT diagnosis (RR 0.69, CI: 0.49–0.97), as did current/prior smokers (RR 0.57, CI: 0.35–0.93). In multivariable analyses, lower CT diagnosis rates were only detected among those having HOPS entry year before 2019 (aRR 0.59, CI: 0.40–0.85) (Supplemental Table 2b).
Syphilis
There were 114 syphilis cases among 2,311 participants and 4,216 syphilis tests completed during the study period. The median number of syphilis tests per participant during both the pre-pandemic and pandemic periods was 1 (IQR 1–2). During the pre-COVID-19 pandemic era, 58 participants had one, 7 had two, and 5 had three or more documented syphilis infections. During the pandemic era, 44 participants had one, 3 had two, and 3 had three or more documented syphilis infections. Overall, the RRs for syphilis test and syphilis diagnosis comparing the pandemic vs. pre-pandemic periods were 0.93 (CI: 0.88–0.99) and 1.08 (CI: 0.98–1.19), respectively (Figure 1). The test RR for pandemic vs. pre-pandemic periods was lower (P< 0.05) for some participant characteristics: male sex, Hispanic/Latino race/ethnicity, having public insurance, being seen in a public clinic, having HOPS entry year before 2019, having baseline CD4 ≥ 500 cells/mm3 or VL < 200 copies/mL, and being ART experienced (Supplemental Table 3a). In multivariable analyses, while the interaction between prior AIDS diagnosis and time period (pandemic vs. pre-pandemic) was significant, due to those with prior AIDS diagnosis trended toward increased syphilis testing rates while those without trended toward decreased testing rates, neither subgroup (i.e., with or without prior AIDS diagnosis) had a statistically different (higher or lower) rate during the pandemic compared to the pre-pandemic time period. In univariable analyses, the pandemic period, was associated with higher rates of syphilis infection for those within the MSM HIV transmission risk group (RR 1.11, CI: 1.00–1.23), having first HOPS visit during 2019–2021 (RR 1.39, CI: 1.08–1.80), having baseline CD4 of 350–499 cells/mm3 (RR 1.29, CI: 1.01–1.66), having baseline VL ≥ 200 copies/mL (RR 1.43, CI: 1.12–1.81), and being ART naïve at baseline (RR 1.54, CI: 1.06–2.23), in comparison to the pre-pandemic period. In multivariable analyses, no differences in rates comparing pandemic versus pre-pandemic periods were found across subgroups (Supplemental Table 3b).
Discussion
This study provides evidence of pandemic-associated ambulatory disruptions in HIV care, namely STI testing and diagnosis. In our diverse multi-site cohort of HIV outpatients, test rates for chlamydia, gonorrhea, and syphilis decreased after the start of pandemic. This was also seen in a national study of chlamydia and gonorrhea testing by Pinto et al., who describe 15% fewer tests reported by end of June 2020, but higher incidence rates7. Pinto et al., note that this drop-off in testing likely reflects a shift from risk-based STI testing to symptomatic testing, which aligned with the CDC recommendations at the time of the stay-at-home orders to defer routine STI screening visits8. Another study in Oregon showed that STI testing rates remained lower than pre-pandemic rates through September 20209. Additionally, investigators reported that chlamydia and early-latent and late-latent syphilis diagnoses decreased dramatically during this time, likely because more asymptomatic cases were missed due to decreases in testing. The decrease in testing for asymptomatic infections could be due to lack of access to testing sites, many of which had closures, had converted mostly to telehealth, or had staff who were re-deployed to COVID-19-related tasks. A national study of STI programs found only 32% of disease intervention specialists (DIS) were available for remote or virtual work during March 2020-June 2020. In-person or field work performed by U.S. DIS workers fell by 83%; 78% of staff had redeployment to COVID-related programs; 20% of STI programs had complete disruptions to operations and were unable to perform STI prevention functions, such as distribution of free condoms; while another 76% of programs reported significant disruptions to operations10. Testing decreases could also have occurred from supply shortages of swabs and reagents, as many suppliers pivoted to increase COVID-19 testing supplies11 Additionally, there were reductions in health-seeking behaviors by some patients concerned with potential COVID-19 exposures. Also, during the early stages of the COVID-19 pandemic, some cities in our study cohort, including Chicago, Denver, Washington D.C., and Philadelphia implemented measures related to deferment of non-urgent medical care, which would apply to asymptomatic STI screenings. In total, these occurrences help to explain the observed STI testing decreases in our cohort.
Studies have found that sexual behaviors to various degrees changed during the pandemic, but there is conflicting information about specific behaviors and for how long any behavioral change lasted. In a survey of MSM in the US during April 2020, half of the respondents reported fewer sex partners12. Additionally, many non-essential businesses, including bathhouses, sex clubs, gyms and social clubs were likely closed during pandemic, which could have affected sexual behaviors and sexual networks. In another study among MSM in the U.S. South, the number of partners, anal sex acts and condomless anal intercourse decreased from February-April 2020, followed by an increase from April to June13. Another cross-sectional survey of MSM conducted during April-May 2020 observed a mean increase of 2.3 sex partners during the COVID-19 lockdown period, compared to the 3 months prior to lockdown, and it correlated with increased substance use and binge drinking during the same period3. MSM comprised 56% of our study population, so the behavioral changes described are not completely generalizable to our study, but it is worth noting that both sexual and social behaviors were in flux during various stages of the pandemic. Unfortunately, decreases in partner services occurred during and after the peak of the pandemic, so objective data to support changing sexual practices and partner services was difficult to attain. In totality, there is no consensus on how changing social and sexual behaviors during and immediately after the pandemic stay-at-home orders affected STI transmission and testing.
Our study showed diagnosis rates for chlamydia, gonorrhea, and syphilis were not statistically different in pre-pandemic vs. pandemic time. Similarly, rate of gonorrhea and primary and secondary syphilis increased and surpassed the previous year by 10% and 7%, as reported in the 2020 Sexually Transmitted Disease Surveillance report, published by the CDC. Meanwhile, chlamydia cases dropped by 13% in 2020, which the surveillance report suggests was due to a decrease in screening, not a reduction in new infections14. Since the pandemic reduced access to STI testing, asymptomatic cases could have been missed and the chlamydia diagnosis rate under captured. We believe that our observed lower rate of chlamydia diagnosis could be more of a surrogate for decreased testing than for changing sexual behaviors, but continued STI surveillance efforts for asymptomatic disease are needed to fully determine the effect of pandemic on STI transmission.
Our study has some limitations. Given disruptions in care, patients could have sought care outside of the HOPS clinics for symptomatic STIs or STI exposures, affecting both STI diagnoses and testing results, and results from care received outside of HOPS clinics may not be systematically available in HOPS records across all sites. Likewise, some providers could have empirically treated patients with oral antibiotics without testing and utilized expedited partner therapy, which would also underestimate testing rates. Possible high rates of asymptomatic STI infections, combined with a lack of information on existence of prior, negative tests, meant we were unable to determine whether initial STI diagnoses were incident infections. Because of the real-world nature of the HOPS medical care and record abstraction data, we could not require that participants had visits or STI tests in both study eras; consequently, asymptomatic STI cases could be missed. Lastly, our findings were based on a convenience sample of patients from eight HIV specialty HOPS clinics, limiting its generalizability to patients in other HIV clinic settings or those not in HIV care.
Despite efforts to engage PWH and prevent interruptions in the HIV care continuum during and after the pandemic, such as the use of telemedicine, there was a decrease in STI testing rates in the HOPS cohort. The loss of clinic-based care for PWH around the time of the pandemic negatively affected engagement and routine screenings, including STI testing, diagnosis and prompt treatment1. The impact of pandemic-associated HIV care continuum disruption will require continued investigation and surveillance to avoid complications of untreated STIs.
Supplementary Material
Acknowledgements
The HIV Outpatient Study (HOPS) Investigators include the following persons and sites:
Jun Li, Kate Buchacz, Alex Ewing, HIV Research Branch, Division of HIV Prevention, National Center for HIV, Viral Hepatitis, STD, and TB Prevention (NCHHSTP), Centers for Disease Control and Prevention (CDC), Atlanta, GA; Cheryl Akridge, Stacey Purinton, Selom Agbobil-Nuwoaty, Kalliope Chagaris, Kimberly Carlson, Qingjiang Hou, Carl Armon, Linda Battalora, Jonathan Mahnken, Cerner Enviza An Oracle Company, Kansas City, MO; Frank J. Palella, Conor Daniel Flaherty, Cheryl Carter- Houston, Feinberg School of Medicine, Northwestern University, Chicago, IL; Cynthia Firnhaber, Barbara Widick, Rosa Franklin, Billie Thomas, Vivent Health, Denver, CO; Jessicamarie Fox, Linda Kirkman, DuPont Circle Physicians Group, Washington, DC; Jack Fuhrer, Linda Ording-Bauer, Rita Kelly, Jane Esteves, State University of New York (SUNY), Stony Brook, NY; Ellen M. Tedaldi, Ramona A. Christian, Faye Ruley, Dania Beadle, Princess Davenport, Lewis Katz School of Medicine at Temple University, Philadelphia, PA; Richard M. Novak, Andrea Wendrow, Stockton Mayer, University of Illinois at Chicago, Chicago, IL; Cynthia Mayer, Karen Maroney, Kimberly Braden, Tori Edwards, Brenda Ware, Chrissy LaPointe, St. Joseph’s Hospital Comprehensive Research Institute, Tampa, FL; Theo Hodge, Benita Viswasam, Washington Health Institute, Washington, DC; Gina Simoncini, AIDS Healthcare Foundation, Philadelphia, PA
Source of Funding:
Funding: Centers for Disease Control and Prevention contract nos. 200–2001-00133, 200–2006-18797, 200–2011-41872, 200–2015-63931 and 75D30120C08752.
Footnotes
Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.
Conflict Of Interest: Gina Simoncini has been a consultant and on the Speakers’ Bureau for ViiV. The other co-authors declare no conflicts of interest.
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