COVID-19 testing capabilities at urgent care centers in states with greatest disease burden

While rapid and accessible diagnosis is paramount to monitoring and reducing the spread of disease, COVID-19 testing capabilities across the U.S. remain constrained. For many individuals, urgent care centers (UCCs) may offer the most accessible avenue to be tested. Through a phone survey, we describe the COVID-19 testing capabilities at UCCs and provide a snapshot highlighting the limited COVID-19 testing capabilities at UCCs in states with the greatest disease burden.


Introduction
While rapid and accessible COVID-19 diagnosis is paramount to monitoring and reducing the spread of disease, COVID-19 testing capabilities across the U.S. remain constrained. For many individuals, urgent care centers (UCCs) may offer the most accessible avenue to be tested. Using a phone survey, we describe the COVID-19 testing capabilities of UCCs in states with the greatest disease burden.

Methods
Our study received non-human research IRB exemption from the Yale School of Medicine and participant consent was not required. We identified ten states with the highest COVID-19 caseload as of March 19, 2020 according to the Centers for Disease Control (CDC) 1 . Using the Urgent Care Association "Find an Urgent Care" directory, we identified all UCCs within the state of interest and assigned each UCC a numeric identifier. A random number generator was used to select for a convenience sample of 25 UCCs per state. If the UCC was not able to be contacted, a new UCC was randomly selected and called. UCCs were classified into independent, hospital/health network, and academic categories.
Using a standardized survey script (Figure 1), trained investigators asked UCC receptionists about COVID-19 testing ability, testing criteria, time to test results, costs of tests and visits for insured/uninsured patients, and test referrals. All 250 calls were made on March 20, 2020 and were limited to 1 minute to minimize occupying clinic resources. Using publicly available data from the United States Department of Agriculture's Economic Research Service (based off the 2010 U.S. Census), we determined urban/rural designation based on UCC zip codes.
Of UCCs that offered testing, 56 (98.2%) required the patient to be symptomatic (typically fever and respiratory symptoms) and 2 (0.4%) required a primary care physician referral. In total, 45 (86.5%) UCCs charged a fee to test uninsured patients, but no UCC could provide a definitive answer regarding test fees for insured patients given the shifting federal legislation. A total of 53 (94.6%) UCCs charged a visit fee in addition to the COVID-19 lab test fee. For the 49 centers that provided the wait time for test results, the median time was 120 hours (interquartile range 96 hours to 144 hours).
Of UCCs that did not offer testing, 97 (51.3%) referred individuals to other clinics that could possibly test for COVID-19, and 37 (24.8%) directly referred individuals to a specific emergency department. Individual-level results for each UCC are available as Underlying data 2 .
All UCCs were located in urban-designated zip codes. 246 (98.4%) UCCs were located in metropolitan areas, while 4 (1.6%) UCCs were located in small towns with an urban cluster.

Discussion
In the 10 states with the greatest COVID-19 caseload, only 23% of UCCs offered COVID-19 testing. Additionally, results would take approximately five days to be processed. Although time to test results at public/state labs are typically 24-48 hours (Table 1), time to test results at UCCs were longer as most samples are sent to external labs. However, it remains unclear whether UCC ability to obtain test samples may be unmatched by the ability to process tests. This finding underscores the importance of point-of-care testing that can rapidly detect COVID-19, particularly because severe disease peaks at approximately ten days from onset of initial symptoms 3 .
Fees and cost-sharing for COVID-19 tests remain unclear. The Families First Coronavirus Response Act, which passed on March 18, mandated all group and individual health plans cover COVID-19 testing and gave states the option to use Medicaid coverage for testing uninsured patients 4 . Although this study could not definitively define test fees, most UCCs stated they would charge test fees, contrary to recent federal regulations, in addition to fees for the urgent care visit itself as of March 20. Test and visit fees at UCCs may discourage patients from seeking COVID-19 testing.
UCCs continue to face several obstacles in their ability to offer COVID-19 testing. Point-of-care rapid testing remains limited, and the necessity to externally process tests delays the receipt of test results. Overburdened healthcare providers and lack of personal protective equipment could also affect availability and costs of testing at UCCs. Our results identify several primary areas of improvement for UCCs offering COVID-19 testing: 1) the adoption of rapid point-of-care

Amendments from Version 1
In order to answer reviewer comments on the relationship between urban versus rural designation on COVID-19 testing availability, we added a variable that characterized each UCC as urban or rural based on UCC zip codes that were cross referenced with data from the U.S. Department of Agriculture's Economic Research Service. We have updated the results to include the urban/rural designation. All UCCs were located in urban-designated areas. However, 4 UCCs were located in a smaller subset of the urban designation called "small towns with an urban cluster." We have updated the discussion section to identify the obstacles that UCCs face in their ability to offer COVID-19 testing. Additionally, we have identified several areas of improvement for UCCs that offer COVID-19 testing.
Any further responses from the reviewers can be found at the end of the article REVISED testing should be implemented and 2) UCCs should follow legislation that patients should not be charged for COVID-testing.
This report has limitations. The small number of UCCs contacted per state may not accurately represent the state's urgent care climate. Additionally, the rapidly changing nature of the COVID-19 pandemic may affect these findings. However, this study serves as an important snapshot that highlights the limited COVID-19 testing capabilities at UCCs in the most heavily burdened states.

Open Peer Review
How did the authors validate the data from the UCCs to ensure no wrong information was conveyed? Even at the same center, two receptionists may give different answers to the same question. Is it possible to double confirm with two different receptionists? ○ As the authors state that UCCs were randomly selected. How to differentiate big city centers vs rural area centers? High burden states still have rural areas that may have a very low incidence of COVID infection that does not supplement with UCCs with test capability. What is the percentage of these UCCs? ○ Based on the above-mentioned reason, wouldn't investigating UCCs in cities with high COVID-19 incidence be a more reasonable design? ○ Lastly, in the discussion part, the authors merely analyzed the results but did not put forward how it can be utilized for improvement. Namely, what's the meaning of this study?

If applicable, is the statistical analysis and its interpretation appropriate? Yes
Are all the source data underlying the results available to ensure full reproducibility? Yes Are the conclusions drawn adequately supported by the results? Partly same question. Is it possible to double confirm with two different receptionists?
We cannot guarantee that receptionists may or may not convey the correct information, but contacting offices in a randomized approach with a large sample has been a validated way to collect survey information. We cannot double confirm with receptionists given the changing landscape since March. However, this caller approach has been used and validated in many our similar survey methodologies: As the authors state that UCCs were randomly selected. How to differentiate big city centers vs rural area centers? High burden states still have rural areas that may have a very low incidence of COVID infection that does not supplement with UCCs with test capability. What is the percentage of these UCCs?
We have added an urban vs rural variable in our analysis based off the UCC's zip code in the 2010 U.S. Census. UCCs were all located in urban-designated areas. The urbandesignation can be broken down into subcategories, and 4 centers were located in smaller towns with an urban cluster. However, these UCCs are still considered urban. It is well known that UCCs tend to locate in wealthier, urban areas.
The results section and data sharing section have been updated accordingly.
Based on the above-mentioned reason, wouldn't investigating UCCs in cities with high COVID-19 incidence be a more reasonable design?
Given that the primary locations of UCCs at the time of the study were in urban metropolitan areas, we feel confident that our sample essentially represented cities with high COVID-19 incidence. Briefly discuss the obstacles to UCCs offering COVID-19 tests.
We have added several statements on the obstacles to UCC testing in 3 rd paragraph of the discussion section.
How does this snapshot in March reflect the situation today in July? Do the authors observe an association between a higher proportion of testing UCCs in March with better COVID-19 control today?
It is difficult to say whether higher availability of testing is associated with better COVID-19 control, since numerous factors affect the ability to control the spread of infection. However, as we continue into an additional wave of COVID-19 infections, sufficient availability of and accessibility to testing remains paramount.

Competing Interests: None
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