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The COVID-19 pandemic, caused by the novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) virus, has negatively affected many aspects of health care, disrupting most routine, nonemergency care. HIV care and prevention programs were no exception. The impact on health care was felt worldwide and across all aspects of the care continuum.1–5 The Global Fund reported that overall HIV testing decreased by 22% in 2020 as compared with 2019 in countries receiving funding while the number of people reached by prevention services dropped by 11%.6 Similar assessments of worldwide interruptions in HIV testing, diagnosis, and initiation of treatment have been reported by The Joint United Nations Programme on HIV/AIDS.7 In the United States (US), a Centers for Disease Control and Prevention (CDC) report from a single national commercial laboratory found approximately 700,000 fewer HIV screening tests, 5000 fewer HIV diagnoses, and 68,000 fewer viral load tests in the first 6 months of the pandemic compared with the same period in 2019.8 Routine clinical visits for people living with HIV (PLWH) were delayed or cancelled nationwide.9 At the Fenway Health Center in Boston, HIV pre-exposure prophylaxis starts declined by 72% and pre-exposure prophylaxis refill lapses increased by 278% from January 1, 2020, to April 30, 2020.10 Despite transitioning to telehealth visits, there are likely downstream effects on diagnosis, retention in care, and viral suppression, with serious implications for ending HIV transmission.11
Routine HIV screening is a key testing strategy endorsed by the CDC as a high impact, cost-effective prevention intervention for increasing the number of PLWH aware of their diagnosis.12–14 Despite the recommendation, universal HIV screening rates remain low in the United States, even in high incidence areas.15 Health care settings that had been able to successfully implement routine HIV screening programs experienced setbacks as resources were shifted to the COVID-19 response.16–18 For instance, the Expanded HIV Testing and Linkage to Care program, a collaboration of 13 sites on the South and West sides of Chicago for routine, opt-out HIV testing, described how most sites saw declines in testing during the pandemic, and overall, the program saw a 49% reduction in testing events from January 1, 2020, to April 30, 2020.18 Multiple other routine screening programs have detailed major declines in testing during the pandemic.16,17 Few feasible and scalable strategies to mitigate routine HIV testing disruptions have been identified, despite recognition that the pandemic is likely to continue to affect health care delivery with subsequent waves of COVID-19 infection.
We previously reported that maintaining routine HIV screening volumes during the COVID-19 pandemic was achieved at a single institution by incorporating phlebotomy and HIV screening into the evaluation and testing of patients with suspected COVID-19 in the ED.19 This approach resulted in a greater number of patients diagnosed with acute HIV infection (AHI).18,20,21 Past work assessing AHIs in a routine testing program in Chicago showed that 95% of all AHIs were diagnosed in the ED setting.22 Furthermore, patients with AHI presented to the ED due to concern for COVID-19 infection because many symptoms of AHI are shared with those of COVID-19.18 Common symptoms of AHI that overlap significantly with those of COVID-19 and other respiratory viral illnesses include fever, headache, myalgias, nausea, vomiting, and diarrhea.23,24 Recognizing signs and symptoms of AHI is important for early diagnosis of HIV, which, coupled with linkage to care and treatment initiation, results in improved patient health outcomes and reduction in transmission events.25
Concurrent testing, or HIV screening paired with a SARS-CoV-2 test, may allow health care settings to maintain testing volumes and provide an opportunity to identify symptomatic patients with HIV presenting with a viral syndrome. A modeling study projecting the impact of COVID-19 on the HIV epidemic in 6 US cities suggested that systematically linking opt-out HIV screening to SARS-CoV-2 testing could result in a reduction in HIV incidence over the next 5 years and reduce health care costs associated with HIV.26 However, there are little real-world data to support the recommendation to perform linked testing for HIV and SARS-CoV-2.
In this study, we assessed concurrent HIV and SARS-CoV-2 testing patterns (HIV and SARS-CoV-2 testing in the same encounter) and the relationship to diagnosis of new and AHIs during the first year of the pandemic at multiple EDs in the Chicago metropolitan area. Cook County, IL, encompassing Chicago, is an area of high HIV prevalence and incidence and a priority jurisdiction for Ending the HIV Epidemic in the US.11,27,28
METHODSA retrospective review of HIV and SARS-CoV-2 testing was conducted at 6 EDs in the greater Chicago metropolitan area of Illinois. Testing data from March 1, 2020, through February 28, 2021, were obtained through electronic medical records (EMRs) from Sites A-E. Owing to a change in EMR platform, data from Site F were only available from September 1, 2020, through February 28, 2021.
Site DescriptionsDuring the study period, HIV testing in the EDs at 5 sites (Sites A, C-F) was triggered by an automatic prompt in the EMR in nursing triage for all persons who met CDC criteria, had no known diagnosis of HIV, and did not opt out of HIV screening.12 Patients were excluded if unconscious or lacked capacity to opt out. At one site with an automated EMR prompt, routine testing was offered regardless of other laboratory tests ordered (Site E), while at the 4 other sites (Sites A, C, D, and F), testing was connected to a blood draw (2 sites offered testing to all patients who required a blood draw [Sites A and F]) and 2 sites provided testing to all patients who had a complete blood count ordered (Sites C and D). More frequent testing was offered for patients presenting for sexually transmitted infection (STI) testing, with signs or symptoms of AHI, reporting condomless sex with multiple partners or injection drug use, who identify as men who have sex with men (MSM), who are victims of sexual assault, or at clinician discretion or patient request. One site (Site F) used an additional EMR algorithm to determine need for more frequent repeat testing based on epidemiologic, behavioral, and social factors associated with HIV transmission.29,30 Among the 6 sites, HIV testing at the site that did not use an automated prompt (Site B) was clinician-initiated on ED patients presenting for symptoms of STIs, acute fever and rash, pneumonia, other signs of immune compromise, all pregnant women, or at clinician discretion or patient request. All sites used fourth or fifth generation HIV-1/2 Ag/Ab combination assays with same-day results available for the screening assay and within 24–48 hours for the confirmatory antibody test. The timing of HIV-1 RNA quantitative PCR results varied site to site. Some delays were experienced due to reagent shortages and excess workload on clinical microbiology laboratories during the COVID-19 pandemic.
Although hospital infection control policies changed through the pandemic, during most of the data collection period, PCR-based SARS-CoV-2 testing at 5 of the sites (Sites B-F) was performed for symptomatic persons and all persons who were admitted to the hospital, regardless of symptoms. One site (Site A) did not routinely screen asymptomatic patients who were being admitted. Three sites were able to provide a breakdown of symptomatic and asymptomatic SARS-CoV-2 tests (Sites C-E).
Data Collection and Statistical AnalysisEach hospital identified ED volume, the total number of HIV screens, SARS-CoV-2 PCR tests, and encounters where concurrent testing occurred. The total number of new HIV diagnoses, including AHI, was collected. Additional data were collected for patients with AHI, including demographics such as age, sex, and race/ethnicity; clinical information such as behavioral factors associated with HIV transmission, reported symptoms, HIV viral load, CD4 count, and suspicion of being infected with SARS-CoV-2; and care continuum information, such as linkage to care and time to treatment initiation.
Proportion of concurrent tests among all SARS-CoV-2 tests was calculated for all sites. Owing to acute HIV diagnosis being a rare event,22 monthly totals from each ED were grouped by quarter. Quarter 1 combined testing from March 2020 through May 2020, Quarter 2 from June 2020 through August 2020, Quarter 3 from September 2020 through November 2020, and Quarter 4 from December 2020 through February 2021. Site F only reported data for Quarters 3 and 4. Considering the number of new HIV diagnoses (both acute and nonacute) and the issue of linearity, the Spearman rank correlation coefficient was used to measure the correlation between both overall testing and the proportion of SARS-CoV-2 tests paired with an HIV test with new and acute HIV diagnoses. To account for the variation in HIV testing volume between EDs, a partial Spearman correlation test controlling for the number of HIV tests was also conducted. We performed a sensitivity analysis including only symptomatic SARS-CoV-2 testing from the 3 sites that provided that information. Statistical analyses were performed in SAS version 9.4 (SAS Institute Inc., Cary, NC) with two-sided P-tests <0.05 considered statistically significant. This study was determined to be exempt from Institutional Review Board (IRB) oversight at the University of Chicago, where data analysis was performed. The IRBs at other participating sites approved this work.
RESULTS Main ResultsA total of 113,645 SARS-CoV-2 tests, 36,094 HIV screens, and 17,469 concurrent tests were performed during the study period. The EDs diagnosed 102 new cases of HIV, with 25 (24.5%) of them AHI (Table 1). Among all newly identified patients with HIV, patients with AHI (21/25) were significantly more likely to be tested for both SARS-CoV-2 and HIV compared with nonacute (29/77) newly diagnosed patients (odds ratio [OR] 8.69; 95% CI: 2.71 to 27.8, P < 0.001). Approximately half (12/25) of patients with AHI indicated upon arrival to the ED they believed they had COVID-19. Of the 4 patients with AHI who did not have a SARS-CoV-2 test, 3 of the patients indicated a recent negative result for COVID-19.
TABLE 1. - Testing Volumes for HIV, SARS-CoV-2, Concurrent Tests, and HIV Infections Diagnosed at Six Chicago-Area Emergency Departments From 3/1/2020 Through 2/28/2021 Site ED ED Volume* HIV Screens SARS-CoV-2 Tests Concurrent Tests Proportion Concurrent Tests† New HIV Diagnoses Acute HIV Diagnoses Site A 64,791 4,285 7,263 1,008 0.1388 16 0 Site B 64,939 1,373 35,292 618 0.0175 8 3 Site C 53,088 4,783 21,870 1,889 0.0864 18 3 Site D 22,432 1,821 10,662 719 0.0674 10 3 Site E 73,363 20,569 30,023 11,129 0.3707 45 15 Site F‡ 19,381 3,236 8,535 2,106 0.2467 5 1 Totals 297,994 36,094 113,645 17,469 0.1537 102 25*ED volume indicates total ED encounters over the data collection period apart from Sites C and D, which reported unique patients seen on a monthly basis aggregated over the data collection period.
†Proportion SARS-CoV-2 tests with a concurrent HIV screening assay.
‡Data provided from September 1, 2020, through February 28, 2021 (Quarters 3 and 4) only.
*n = 21; 4 patients missing CD4 counts.
†Patient tested for both SARS-CoV-2 and HIV in the same encounter.
GI, gastrointestinal; LTC, linkage to care; SOB, shortness of breath; VL, viral load.
Most of the AHI patients were male (88%) and African American (84%) with a median age of 27 years at the time of diagnosis (Table 2). There were 14 MSM (56%), 5 heterosexual men (20%), 3 bisexual men (12%), and 3 cis-gender heterosexual women (12%). Common clinical symptoms reported in the ED were muscle aches/pains (52%), gastrointestinal issues (48%), fever (48%), and pharyngitis (40%). Less common symptoms were weight loss (20%), shortness of breath (16%), rash (12%), and lymphadenopathy (12%). The median initial viral load of all patients with AHI was 4,120,000 copies/mL (interquartile range [IQR]: 953,000–6,000,000), with an initial median CD4 count of 457 cells/mm3 (IQR: 281–537). The median time to linkage of care and initiation of antiretroviral therapy (ART) was 3 days with 75% of acute patients linked to care within the first 2 weeks of their positive HIV screening assay. A total of 17 of the 25 patients achieved documented viral suppression (<200 copies/mL), and of those 17 patients, the median time to suppression was 71 days.
A moderately strong, positive correlation was found between total HIV testing volume and the number of new HIV infections (r = 0.664, P = 0.001; Fig. 1). The proportion of patients tested for both SARS-CoV-2 and HIV had a medium-strength correlation with the number of AHIs diagnosed although was not statistically significant (r = 0.371, P = 0.089; Fig. 2). When controlling for the differences in HIV testing among the different EDs, however, there was no relationship between concurrent testing and AHIs (P = 0.593). There was no relationship between the proportion of concurrent tests and nonacute newly diagnosed HIV infections (r = 0.183, P = 0.416).
FIGURE 1.: Number of HIV screening assays and new HIV diagnoses by site. * Data provided from September 1, 2020, through February 28, 2021 (Quarters 3 and 4) only.
FIGURE 2.: Spearman correlation between concurrent SARS-CoV-2 and HIV testing proportions* and quarterly diagnosis of acute HIV infection (AHI). *Proportion SARS-CoV-2 tests with a concurrent HIV screening assay.
Symptomatic Sensitivity AnalysisData restricting SARS-CoV-2 testing to only those labeled as symptomatic for COVID-19 were available for further analysis from Sites C, D, and E. Overall, 58.2% of tests were symptomatic, 32.4% were asymptomatic tests, and 9.4% were undefined tests (Table 3). The proportion of SARS-CoV-2 testing that was symptomatic (compared with asymptomatic or undefined testing) was variable between Site C (76.2%), Site D (67.1%), and Site E (41.9%). When examining only symptomatic tests between the 3 sites, the proportion of concurrent testing was strongly correlated with the number of AHIs diagnosed (r = 0.869, P < 0.001). After adjusting for HIV screening volume at each site, the relationship was moderately correlated and not statistically significant (r = 0.590, P = 0.056). In addition, in patients whose original HIV screening assay was linked to a SARS-CoV-2 test, AHIs were significantly more likely to be linked to a symptomatic SARS-CoV-2 screen versus an asymptomatic one compared with the nonacute new diagnoses (92.9% vs 57.9%, P = 0.048).
TABLE 3. - SARS-CoV-2 Symptomatic and Asymptomatic Testing Information for a Subset of Sites Site ED HIV Screens SARS-CoV-2 Tests Symptomatic SARS-CoV-2 Tests Asymptomatic SARS-CoV-2 Tests Undefined SARS-CoV-2 Tests Proportion Symptomatic SARS-CoV-2 Tests with an HIV Screen Site C 4,783 21,870 16,659 2,994 2,217 0.0846 Site D 1,821 10,662 7,154 2,900 608 0.0718 Site E 20,569 30,023 12,594 14,380 3,049 0.3783 Totals 27,173 62,555 36,407 20,274 5874 0.1837Data from the CDC and Chicago Department of Public Health surveillance reports27,31 indicate a decline in new diagnoses of HIV in 2020. While on the surface this seems to bring us closer to our goal of HIV elimination by the year 2030, it remains uncertain whether this reflects a true decrease in transmission versus fewer new diagnoses due to disruption of testing services. Reported data indicate that sexual activity among MSM in the United States initially decreased during the peak of COVID-19 shutdowns and social distancing requirements but increased thereafter.32,33 Similarly, national case reporting of bacterial STIs decreased dramatically in March and April of 2020 as compared with the same time in 2019, likely in part due to decreased screening; however, cases of gonorrhea and syphilis increased later in 2020, surpassing 2019 levels.34,35 Syphilis cases rose during the early pandemic at one Chicago program that maintained screening rates.36 In this study, we found that higher HIV testing volume was positively correlated with the number of new diagnoses in 6 EDs across Cook County, IL. Our findings, along with the widespread descriptions of decreased access to HIV testing, prevention, and care services,8–10,32,33,37 would suggest that observed trends in HIV transmission during the COVID-19 pandemic are likely due to diminished testing rather than fewer transmission events, particularly in areas of high HIV prevalence. Real-time data on HIV diagnoses, similar to weekly reports on COVID-19 and influenza,38–40 would be helpful to inform HIV testing, treatment, and prevention programs and should be possible given the will.
Although higher proportion of concurrent SARS-CoV-2 and HIV testing was not correlated with a higher number of overall new HIV diagnoses after accounting for testing volumes in the current analysis, strategies that increase the number of HIV screening assays performed will identify more cases. In this study, the site that performed the most HIV screening tests identified the highest number of new cases of HIV. Furthermore, performing symptomatic SARS-CoV-2 testing with HIV screening was correlated with the number of AHIs detected. A testing strategy that links HIV screening to that of COVID-19 and other viral illnesses will likely increase the volume of HIV screening and result in more diagnoses of HIV and AHI in certain geographic areas. Indeed, there may be potential benefits of linking HIV screening to other viral syndromes including respiratory viruses, infectious gastroenteritis, and acute mononucleosis to expand this approach beyond the COVID-19 pandemic, given the variable presentation of AHI and recent uptick in respiratory and other viral illnesses.39 Among the AHIs identified, patients were rapidly linked to care and started on ART, primarily because of strong partnerships between ED and HIV care programs.41,42
We saw differences across sites in concurrent screening rates and associations with new and acute diagnoses. For instance, site F did not follow the trends seen in other sites where an increase in concurrent testing was associated with a higher number of AHIs identified. It is not clear whether this is due to differences in patient population or perhaps if Site F's data were skewed due to the inclusion of just 6 months of data. Across all sites, the proportion of SARS-CoV-2 tests with a concurrent HIV test was low, even when limited to testing performed for symptomatic individuals. The results may have been different had all patients with viral symptoms been tested for HIV. Site differences in concurrent testing rates can be informed by methods of routine HIV screening. At several sites, HIV screening is performed only when blood is drawn for other purposes. This may have resulted in lower concurrent testing for persons with respiratory symptoms at these sites but does not fully account for all differences. Many patients with viral symptoms do not otherwise require a blood draw, and this may disqualify them for routine screening at some sites.
Although there are challenges to ED-based screening programs, the ED remains the highest yield health care setting for identifying PLWH, both undiagnosed and out of care.22,43 To link HIV testing with that for SARS-CoV-2 and other respiratory viral illnesses, opt-out HIV testing in the ED will need to be expanded beyond patients requiring blood draws. For established routine testing programs that use this method, truly linking HIV testing with that for acute respiratory illnesses will require effort to implement. Given that many people with limited access to care use the ED as their primary source of care, altering workflows to include laboratory draws for HIV testing for all patients, especially those with viral symptoms, is a critical strategy to reach vulnerable patients in areas of high HIV transmission. ED and institutional buy-in would be necessary to support the additional laboratory draws, EMR modifications, and staff training needed to adopt and sustain such an approach. Yet, the site with the highest volume of testing in our study (Site E) has previously shown that such an approach is possible in a high-volume urban ED with minimal workflow disruption and is sustainable even in the face of a pandemic.19 In this model, all patient notification and linkage is managed by the HIV care program, freeing the ED to prioritize testing.42 On a policy level, HIV testing at institutions in EHE priority jurisdictions may be incentivized through improved reimbursement structures or by establishing quality measures for HIV testing in the ED as part of value-based care.44,45
As the COVID-19 public health emergency in the United States has ended,46 we must consider how we can leverage the COVID-19 response to mitigate setbacks toward the goal of HIV elimination and lend urgency to improving early diagnosis and care continuum entry, particularly in high priority jurisdictions for the National Ending the HIV Epidemic.11,28 Increased access to HIV home testing and expanded telehealth options for retention in care are a few examples of positive advancements resulting from the pandemic.34,47–49 Systematically linking HIV testing and SARS-CoV-2 testing in the ED may be one method by which to increase the proportion of PLWH who are aware of their diagnosis and in care. Modeling suggests that linked, opt-out HIV testing with SARS-CoV-2 testing is a cost-effective way to reduce incidence of HIV, if patients are linked to care and start ART.26 Others have called for using the massive COVID-19 contact tracing workforce to address other health conditions such as HIV by pairing COVID-19 contact tracing with HIV testing, which would reach far into the community.49,50 If adopted in a widespread manner, these strategies may help achieve HIV elimination goals.11,13,26
This study has several limitations. Given that the analysis was limited to one geographic area, the results may not be widely applicable as local HIV epidemics vary quite widely. One site was only able to provide data for 6 months due to a change in EMR and did not include the first 6 months of the pandemic. Furthermore, we had data on symptomatic testing from only a subset of sites. We were also unable to reliably collect socioeconomic data of those tested from all sites. These data collection limitations may have affected the ability to understand patterns of testing and diagnosis as the pandemic progressed and across patient populations. Several sites have HIV testing linked to a blood draw or complete blood count to optimize ED workflow, which may limit the amount of HIV testing performed, particularly with patients who may otherwise only require samples for respiratory viruses. Although much symptomatic testing for COVID-19 occurred in outpatient and drive-thru settings, these sites often lacked the capacity to perform concurrent blood-based HIV testing; thus, our analysis is limited to the ED setting. It is possible we would see different results if linked testing were extended to all sites performing large volumes of SARS-CoV-2 testing in areas of high HIV incidence and prevalence.
Centered in the high priority area of Cook County, IL, over the first year of the COVID-19 pandemic, our study found that higher volume of ED HIV testing resulted in more HIV diagnoses and that symptomatic, concurrent SARS-CoV-2 and HIV testing was correlated with diagnosis of AHI. Moving forward, it should be a priority to study how linked testing for HIV and respiratory viruses enhances process outcomes for HIV screening programs (number of screens and number of new and acute diagnoses) and clinical outcomes (rapid linkage to care and initiation of ART). This will be important in the near-term as COVID-19 transmission continues and may also inform practices during respiratory and other viral outbreaks in a postpandemic world.
ACKNOWLEDGMENTSFOCUS funding supports HIV, HCV, and HBV screening and linkage to the first medical appointment after diagnosis; FOCUS funding does not support any activities beyond the first medical appointment and is agnostic to how FOCUS partners handle subsequent patient care and treatment.
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