Abstract
Adolescents and young adults (AYAs) living with HIV have high rates of co-sexually transmitted infections (STIs). During the coronavirus disease (COVID) pandemic, STI prevention strategies, including access to testing/treatment facilities, availability of health care workers, and condom availability, may have decreased. This study aimed to determine if differences in STI incidence for first infection and reinfection existed between the pre-COVID and COVID eras in a cohort of AYAs living with HIV in Atlanta, GA. Retrospective chart review was conducted for all patients between ages 13 and 24 at the Grady Ponce Clinic. Two eras were identified: a pre-COVID era (January 1, 2009–December31, 2019) and a COVID era (January 1, 2020–June 30, 2021). STIs recorded included gonorrhea, chlamydia, human papillomavirus, syphilis, trichomonas, herpes simplex virus, lymphogranuloma venereum, hepatitis C, bacterial vaginosis, and chancroid. First and recurrent incidence rates for any STIs were reported. Our sample included 766 sexually active AYAs with HIV. A total of 721 patients were included in the pre-COVID era and 583 (80.9%) had at least one STI. A total of 337 patients were included in the COVID era, and 158 had at least one STI (46.9%). The overall first STI incidence rate increased from 42.47 to 58.67 per 100 person-years (PY) and the recurrent STI incidence rate increased from 121.50 to 169.85 per 100 PY from the pre-COVID to the COVID era (p < 0.001). Our study demonstrated significantly higher incidence rates of first and recurrent STIs in AYAs living with HIV in the COVID era. We urge continuation of existing STI prevention programs to avoid secondary clinical and economic adverse effects of increased infections.
Introduction
The emergence of coronavirus-19 (COVID) in late 2019 led to an overwhelming burden on the health care system in the United States and around the world, leading to a disruption of sexually transmitted infection (STI) prevention services. The government and health authorities responded to the pandemic by implementing a range of measures, such as lockdowns, travel restrictions, and social distancing policies, to contain the spread of the virus. 1,2 In addition, health care resources, including personnel, equipment, and funding, were redirected toward pandemic response activities, such as testing, contact tracing, and vaccine distribution. Although these measures were necessary to mitigate the spread of COVID, the diversion of attention and resources from other public health needs, particularly STIs, raises concerns about the potential long-term consequences on STI prevention and control efforts. 3 In the United States, there was an unintended upsurge of STIs during the pandemic. In a large cohort of pediatric patients with and without human immunodeficiency virus (HIV), Bonett et. al found that adolescent STI and HIV testing decreased during the pandemic with more positive tests compared with a pre-COVID baseline. 4 There were many confounding factors in collecting adequate information that led to a decrease in STI and HIV testing across all age groups and in HIV seropositive and seronegative individuals. STI testing was underutilized in the early pandemic leading to unexpected changes and disruptions in STI patterns. 5 In a study of young adults, earlier phases of the pandemic had a lower amount of STI testing than later phases. 6
Adolescents and young adults (AYAs) are at high risk of STIs due to various factors, including engaging in risky sexual behaviors, lack of condom use, and limited health care seeking behavior. 7,8 In 2018, the CDC estimated that 1 in 5 people in the United States were living with an STI, with nearly half of new STIs diagnosed in youth aged 15–24 years. 9 AYAs living with HIV are at even higher risk of developing co-STIs, especially in patients with horizontal acquisition and noncontrolled HIV due to limited access to sexual health care. 10 –12 In patients with HIV, co-STI is associated with lower CD4 T cell counts and higher viral loads, leading to further STI transmission. 13,14
The CDC’s Sexually Transmitted Disease Surveillance report for 2021 also indicated a drop in Chlamydia trachomatis (CT) cases between 2019 and 2021.15 Initially, both Neisseria gonorrheae (GC) and primary and secondary syphilis cases declined during March and April of 2020, but subsequently exhibited a surge, surpassing the rates observed in 2019.16 CT cases, which are more likely to be asymptomatic, may not have been screened as extensively as GC and syphilis cases, potentially leading to a misrepresentation of the true incidence of STIs during the pandemic. Studies in HIV seronegative adolescents have shown that risky sexual behaviors did not decrease during the pandemic despite stay-at-home orders being in place. 15 Hong et al, reported that men who have sex with men (MSM) aged 13–18 years continued to engage in condomless anal sex during the pandemic despite a significant decrease in HIV testing for this group. 16
It remains unclear how the pandemic affected AYAs living with HIV. In a survey of physicians who care for adolescents, 59% reported a decrease in adolescents seeking care at any point during the pandemic. 17 A COVID impact survey conducted on MSM found that patients living with HIV reported a decrease in HIV-related care visits. 18 Pandemic-induced disruptions to STI prevention and control efforts may have disproportionately affected this population, potentially exacerbating existing health disparities and increasing the potential for HIV transmission.
The Grady Ponce Center (GPC) is the main clinic and referral site for AYAs living with HIV in the metropolitan Atlanta area and one the biggest pediatric and adolescent HIV clinics in the country. The majority of patients at GPC are Black MSM who were horizontally infected with HIV. Rates of STIs in AYAs with HIV at the GPC are high and have been reported by our group previously. 11,12 The aim of this study was to determine differences in STI incidence rates for first and recurrent infections that may exist between the pre-COVID and COVID eras in a cohort of AYAs living with HIV in Atlanta, Georgia.
Methods
Study participants
Retrospective chart review was conducted on all patients at the GPC from January 1, 2009, to June 30, 2021. All patients 13–24 years of age with HIV who self-identified as ever being sexually active and had at least one visit to the GPC over the study period were included. Patients who self-identified as not yet having their sexual debut were excluded. This study received approval from the Institutional Review Boards of both Emory University and Grady Health System.
Data collection
All data were collected using the electronic medical record and entered into REDCap, a standardized online research database hosted at Emory University. 19 Manual chart extraction was completed for encounters before 2011, when the electronic medical record was not yet utilized at the GPC. Data were collected on demographics, HIV infection, including date of diagnosis and mode transmission, self-reported sexual history, and STI events. The STIs considered in this study included the following: GC, CT, syphilis, human papilloma virus (HPV), herpes simplex virus (HSV), trichomonas, hepatitis C (HCV), lymphogranuloma venereum (LGV), bacterial vaginosis (BV), and chancroid. For each STI event, data were collected on patient-reported recent sexual activity (since the last medical visit), signs and symptoms of infection, anatomical sites tested, site positivity, and treatment received.
Definitions
GC: positive culture or nucleic acid test from throat, rectal, and urogenital specimens. CT: positive nucleic acid test from throat, rectal, and urogenital specimens. Syphilis: positive screening with rapid plasma reagin (RPR) and confirmatory treponemal testing. HPV: abnormal anal or cervical Pap smear or clinical presentation of anogenital warts (HPV cotesting is not routinely done in this population). HSV: positive clinical diagnosis or direct fluorescent antibody, culture, or nucleic acid testing. Trichomonas: positive wet mount or urine analysis showing trichomonas or positive nucleic acid testing. HCV: positive blood serology with confirmatory nucleic acid testing. LGV: positive clinical diagnosis (large inguinal adenopathy and painful/bloody stools) with or without positive serology for Chlamydia trachomatis serovars L1, L2, and L3. BV: positive clinical diagnosis (fishy odor and cervical discharge) in addition to clue cells on wet mount or Pap smear. Chancroid: positive clinical diagnosis (painful genital ulcer with suppurative inguinal adenopathy).
Incident Infection
The first occurrence of a particular STI during each era. For HSV, incident infection was the first episode of clinical symptoms during the study period without a documented history of infection. Similarly, for HPV, incident infection was the first abnormal Pap smear or occurrence of anogenital warts during the study period without a documented history of infection.
Reinfection
Subsequent episodes of the same STI in an individual following resolution of a previous episode during each era. Only single events were recorded for chronic conditions such as HSV and HPV. For syphilis infection, resolution was determined by a '4-fold drop in RPR titer and reinfection was determined by a 4-fold increase in RPR titer or a 2-fold increase in RPR titer with high clinical suspicion and treatment by a provider. Resolution for the remaining STIs was determined by receipt of appropriate treatment or the passage of 3 months after the date of STI onset if there was no documentation of treatment in the medical chart.
Statistical Analyses
Statistical analyses were performed in SAS v.9.4 (Cary, NC), and statistical significance was evaluated at the 0.05 threshold. Baseline demographic and longitudinal clinical STI data were summarized using means and standard deviations for continuous variables and frequencies and percentages for discrete characteristics. In the overall sample, STI incidence was calculated two ways. The first method considered only the first occurrence of any and individual STIs during the study period; the second method calculated STI incidence only for recurrent infection, occurring after the first incident STI. For first occurrence, follow-up time was calculated as time from initial observation (i.e., minimum of 13th birthday, January 1, 2009, and first clinic visit date) to the date of first infection, for the STI(s) of interest. For recurrent infection, follow-up time was calculated as the difference between the patient’s last observation (i.e., minimum of 25th birthday, December 31, 2018, and last clinic visit date) and the patient’s first observation and then subtracting from that value any follow-up time when the patient was infected with the STI(s) of interest. In each case, incidence was calculated by dividing the number of qualifying incident STIs by the cumulative follow-up time, corresponding to the STIs of interest, and presented as a rate per 100 person-years (PY). Differences in STI incidence rates between pre-COVID and COVID eras were quantified using incidence rate ratios per 100 PY, with two-sided exact mid-P 95% confidence intervals and p-values. Year-to-year first incidence rate ratios per 100 PY were also calculated from 2009 to 2019.
Results
A total of 766 AYAs living with HIV were included in the analysis. The pre-COVID era included 721 patients—the majority were male [521 (72.3%)], Black [659, (91.4%)], and had a mean age of 18.84 (±SD 2.85). The COVID era included 337 patients—the majority were male [230 (68.2%)], Black (289, 86%), and had a mean age of 18.24 (± SD 3.14) (Table 1).
Demographics by Cohort
SD, standard deviation.
First incidence
Table 2 demonstrates first incidence rates for the pre-COVID and COVID eras. In the pre-COVID era, 583 (80.9%) patients were diagnosed with at least one STI. HPV was the most common incident STI (379, 52.6%), followed by GC (343, 47.6%) and CT (319, 44.2%). This group had a cumulative incidence rate of 42.47 STIs per 100 PY (95% confidence interval [CI]: 39.13–46.03). In the COVID era, 158 (46.9%) patients were diagnosed with at least one STI. GC was the most common STI (90, 26.7%), followed by syphilis (65, 19.3%) and CT (59, 17.5%). This cohort had a cumulative incidence rate of 58.67 STIs per 100 PY (95% CI: 50.05–68.37). The rate ratio of first STI incidence rates between the pre-COVID and COVID eras was 1.38 (95% CI: 1.16–1.65). Therefore, the overall incident STI rate was 38% higher in the COVID era compared with the pre-COVID era. For individual STIs, there was a statistically significant increase in STI incidence rates between the two eras for GC, trichomonas, and syphilis (Table 2).
First STI Incidence by COVID Eras with Rate Ratios, 95% CI, and p-Values
A total of 766 patients in the database—patients may appear in both eras (STI follow-up clock restarts on January 1, 2020).
A total of 2,929 qualifying STIs in the database, 2,595 in pre-COVID and 334 in COVID.
Follow-up rules.
• Maximum of patients’ HIV diagnosis date, 13th birthday, or January 1, 2009, in the pre-COVID era and HIV diagnosis date, 13th birthday, or January 1, 2020, in the COVID era, were considered the respective
• Minimum of patients’ last clinic visit, 25th birthday, or December 31, 2019, in the pre-COVID era and patients’ last clinic visit, 25th birthday, or June 30, 2021, in the COVID era, were considered the respective
• STIs that occurred (or recurred) in this window were counted and corresponding follow-up times calculated.
• STI, sexually transmitted infection; CT, Chlamydia trachomatis; GC, Neisseria gonorrheae; HPV, human papilloma virus; HSV, herpes simplex virus; HCV, hepatitis C; LGV, lymphogranuloma venereum; BV, bacterial vaginosis; CI, confidence interval.
p-values are presented in boldface to emphasize their significance within the context of the analysis.
Reinfection
The reinfection rate during the pre-COVID era for any STI was 120.62 per 100 PY (95% CI: 114.79–126.67). In the COVID-era, the reinfection rate was 174.16 per 100 PY (95% CI: 148.02–203.64), yielding a rate ratio of 1.44 (95% CI: 1.22–1.71) between the two eras. Reinfection rates are demonstrated in Table 3. While the rate of developing any reinfection of STI was significantly higher in the COVID era compared with the pre-COVID era, no individual STIs showed significantly higher rates of reinfection.
Recurrent STI Incidence by COVID Eras with Rate Ratios, 95% CI, and p-Values
p-values are presented in boldface to emphasize their significance within the context of the analysis.
A total of 537/721 (74.5%) of pre-COVID patients had at least one recurrent STI (1,583 recurrent STIs).
A total of 147/337 (43.6%) of COVID patients had at least one recurrent STI (151 recurrent STIs).
• STI, Sexually transmitted infection; CT, Chlamydia trachomatis; GC, Neisseria gonorrheae; HPV, human papilloma virus; HSV, herpes simplex virus; HCV, hepatitis C; LGV, lymphogranuloma venereum; BV, bacterial vaginosis; CI, confidence interval.
Year-to-Year
Looking at the first STI incidence rates from year-to-year during the last decade in the pre-COVID era (2009–2019), we demonstrate that rates increased in the second half of the decade (starting in 2014) and do not differ significantly from the COVID era rates (Table 4).
To be included in a yearly calculation, a patient had to have a study start date on December 31st or sooner of the year of interest and a study end date during or after the year of interest (i.e., patients who had study start dates after the year of interest or study end dates before the year of interest were removed).
Follow-up spanned January 1st through December 31st for the year of interest and restarted each year.
For example, for a patient who had a same STI in different years (e.g., gonorrhea in 2018 and 2019), each gonorrhea would be separately counted as a “first STI” for respective years, 2018 and 2019.
• STI, sexually transmitted infection; CT, Chlamydia trachomatis; GC, Neisseria gonorrheae; HPV, human papilloma virus; HSV, herpes simplex virus; HCV, hepatitis C; LGV, lymphogranuloma venereum; BV, bacterial vaginosis.
Discussion
This study represents the impact of the COVID pandemic on rates of co-STIs among AYAs living with HIV. Our data reveal a significant increase in the incidence rates of co-STIs in the COVID era compared with the pre-COVID era. In particular, an increase in syphilis and GC cases played a significant role in driving the overall rise in initial STIs with CT, trichomonas, and HCV also increasing during the COVID era. Similar trends have been reported in individuals without HIV. 20 –24 The incidence of reinfection with any STI significantly increased in the COVID era. Meaning, there was a higher risk of developing any STI after already having an STI in the COVID era compared with the pre-COVID era. Of note, no particular STI had a significantly higher reinfection rate between the 2 eras. Previous studies have shown an increase in syphilis reinfection rates in AYA HIV+ men before the pandemic. 25 Our study did not find that reinfection rates for syphilis increased as a result of the COVID pandemic. However, we do see similar trends in reinfection rates for syphilis in the pre-COVID era.
This reported increase in STIs is likely multi-factorial, with disruptions in health care services playing a significant role. This led to a decrease in screening and treatment of asymptomatic STIs 16,22,26 –29 as telehealth services were favored over in-person visits. In addition, shortages of GC and CT diagnostic testing kits occurred due to the prioritization of resource allocation for COVID testing. 3,30 Despite these challenges, STI rates increased in our population, raising concerns that numerous infections could have been missed.
Several additional factors may have played a role in the significantly higher STI rates seen in our study, particularly regarding shifts in sexual behavior among AYAs during the pandemic. This period saw a reduction in the availability of PrEP services 31 and a decline in condom usage. 32 This coupled with the increased drug and alcohol consumption resulting from isolation 33 could have significantly contributed to increased STIs. In a survey of predominantly HIV-negative MSM, Stephenson et al. found that men reported an increase in the number of sexual partners and anal sex partners when comparing the pre-COVID and COVID eras. Although stay-at-home orders were in place, survey respondents largely did not agree that reducing the number of sexual partners is important to reduce the spread of COVID. 34 In a Swiss survey of sexually active MSM living with HIV, 14% of respondents reported an increase in sexual partners during the pandemic when compared with before. 35 This low perceived risk of COVID infection from sexual encounters coupled with more free time due to stay-at-home orders could have led to increased risky sexual behaviors.
Further, decreased access to prevention and health education typically provided by schools, health departments, and community organizations during the pandemic likely impacted STI rates. The CDC reports that AYAs who receive comprehensive sexual health education are more likely to delay the initiation of sexual intercourse, have fewer sex partners, have fewer experiences of unprotected sex, and have increased use of protection. 36,37 It is unclear how shifting to online learning impacted the effectiveness of these sexual health programs. However, disruption of in-person sexual health education likely contributed to the increase in STI rates seen in our population. In addition, many health care facilities and public health organizations reduced in-person visits to minimize the risk of COVID transmission, leading to challenges in STI contact tracing. In a survey of 59 CDC-funded STI prevention programs, 3 96% of respondents reported reassignment of staff from STIs to COVID efforts. This significantly impacted STI prevention programs, including decreased partner notification and STI field testing.
Lastly, while the transition to telehealth services was necessary to safely conduct medical visits during the pandemic, it challenged health care accessibility and confidentiality for AYAs. In a study investigating adolescent and parent perception of telehealth visits, adolescents reported concerns for privacy, specifically relating to the location of the visit and ability of family members to overhear them. Although alone time with a provider increased comfort in discussing sensitive issues, only 31% of adolescents reported access to this environment. 38 Therefore, telehealth visits may miss key sexual health information that is essential to screening and diagnosing STIs.
It is intriguing to note that when the data from the pre-COVID era were analyzed by year, we observed a substantial increase in the incidence rates of STIs after 2014, which were comparable with those observed during the COVID era. The lower rates before 2014 may have played a role in accounting for the difference seen between the two eras. Therefore, it is essential to consider alternative explanations beyond the COVID pandemic for the discrepancy seen between the eras. Factors such as changes in teenage sexual behaviors, increased accessibility to internet dating sites, and various social and behavioral factors may provide a more comprehensive explanation for this shift in rates.
Our study includes several limitations. First, due to the retrospective nature, we are limited to information documented in the medical chart. Despite manual chart extraction before 2011, some data were not available for the study team to review. Second, we run the risk of patients seeking care at other clinics, however, this is unlikely because the GPC is the main referral site for AYAs with HIV in the metropolitan Atlanta area. Third, some of the HPV and HSV cases reported in the study period may have truly been prevalent before the study period despite being newly diagnosed. Fourth, we must note that the increase in first STI incidence rates seen in the COVID era may also have increased year to year as a result of our aging patient population and changes in sexual activity with age. Fifth, the COVID era had a smaller follow-up time when calculating incidence per 100 PY and may have overestimated the incidence rates for first and recurrent infections. Lastly, these data were extracted from a single HIV center with predominantly Black, horizontally infected MSM, which may limit the generalizability of our findings to other populations.
In conclusion, AYAs with HIV are at high risk of first and recurrent co-STIs. Our study found significantly higher rates of first and recurrent STIs in the COVID era compared with the pre-COVID era for AYAs with HIV. Disruptions to STI prevention programs, including decreased STI screenings, contact tracing, and comprehensive sexual education, transition to telehealth services over in-person visits, and overall limited access to health care during the COVID pandemic significantly impacted AYAs living with HIV and likely contributed to the increased rates of STIs seen in our study. It is crucial to continue proactive efforts aimed at decreasing STIs within this high-risk population. As we transition to a post-pandemic era, it is vital to understand the consequences of these disruptions and emphasize the need to continue to provide comprehensive sexual health for these individuals.
Footnotes
Author Contributions
F.K. was involved in investigation, visualization, and writing—original draft. L.L. was involved in conceptualization, methodology, investigation, and writing—review and editing. A.S. was involved in conceptualization, methodology, and investigation. S.G. was involved in formal analysis, software, data curation, and writing—review and editing. A.C.G. was involved in conceptualization, methodology funding acquisition, supervision, and writing—review and editing.
Author Disclosure Statement
No competing financial interests exist.
Funding Information
No funding was received for this article.
