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. 2020 Aug 20;8(10):3378–3387.e11. doi: 10.1016/j.jaip.2020.07.057

Pediatric Asthma Health Care Utilization, Viral Testing, and Air Pollution Changes During the COVID-19 Pandemic

Kiara Taquechel a,, Avantika R Diwadkar b,, Samir Sayed a,, Jesse W Dudley c, Robert W Grundmeier c,d, Chén C Kenyon d,e, Sarah E Henrickson a,d,f,∗,, Blanca E Himes b,∗∗,, David A Hill a,d,f,∗,
PMCID: PMC7438361  PMID: 32827728

Abstract

Background

The coronavirus disease 2019 (COVID-19) pandemic caused dramatic changes in daily routines and health care utilization and delivery patterns in the United States. Understanding the influence of these changes and associated public health interventions on asthma care is important to determine effects on patient outcomes and identify measures that will ensure optimal future health care delivery.

Objective

We sought to identify changes in pediatric asthma-related health care utilization, respiratory viral testing, and air pollution during the COVID-19 pandemic.

Methods

For the time period January 17 to May 17, 2015 to 2020, asthma-related encounters and weekly summaries of respiratory viral testing data were extracted from Children's Hospital of Philadelphia electronic health records, and pollution data for 4 criteria air pollutants were extracted from AirNow. Changes in encounter characteristics, viral testing patterns, and air pollution before and after Mar 17, 2020, the date public health interventions to limit viral transmission were enacted in Philadelphia, were assessed and compared with data from 2015 to 2019 as a historical reference.

Results

After March 17, 2020, in-person asthma encounters decreased by 87% (outpatient) and 84% (emergency + inpatient). Video telemedicine, which was not previously available, became the most highly used asthma encounter modality (61% of all visits), and telephone encounters increased by 19%. Concurrently, asthma-related systemic steroid prescriptions and frequency of rhinovirus test positivity decreased, although air pollution levels did not substantially change, compared with historical trends.

Conclusions

The COVID-19 pandemic in Philadelphia was accompanied by changes in pediatric asthma health care delivery patterns, including reduced admissions and systemic steroid prescriptions. Reduced rhinovirus infections may have contributed to these patterns.

Key words: Asthma, COVID-19, Pollution, Telemedicine, Respiratory virus

Abbreviations used: CHOP, Children's Hospital of Philadelphia; COVID-19, Coronavirus disease 2019; ED, Emergency department; EPA, Environmental Protection Agency; IFV-A, Influenza virus A; IFV-B, Influenza virus B; PM2.5, Particulate matter less than 2.5 microns; PM10, Particulate matter less than 10 microns; RSV, Respiratory syncytial virus; RV, Rhinovirus; SARS-CoV-2, Severe acute respiratory syndrome coronavirus 2; VTM, Video telemedicine


What is already known about this topic? The coronavirus disease 2019 pandemic caused dramatic changes to daily routines and health care delivery in the United States.

What does this article add to our knowledge? Coronavirus disease 2019 public health interventions were accompanied by a reduction in pediatric asthma encounters and systemic steroid prescriptions. Decreased rhinovirus infections may have contributed to this apparent reduction in asthma exacerbations, although changes in 4 criteria air pollutants were not significantly different than historical trends.

How does this study impact current management guidelines? Our findings reinforce the value of preventative measures for asthma control, especially those designed to limit transmission of respiratory viruses.

Introduction

Coronavirus disease 2019 (COVID-19), an illness caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), arose in late 2019 and rapidly spread around the world. By June 2020, more than 9 million cases and 469,000 deaths had been reported worldwide, with 2.3 million cases and 122,000 deaths in the United States.1 In response to COVID-19,2 health care systems reoriented their delivery structures to prepare for a dramatic increase in COVID-19 cases while attempting to shield unaffected individuals from infection. Simultaneously, various local and national public health interventions designed to limit viral transmission were enacted. At Children's Hospital of Philadelphia (CHOP), the first COVID-19 patient tested positive for SARS-CoV-2 on March 17, 2020. On this date, all nonessential businesses in Philadelphia were prohibited from operating in person.3 Subsequently, the city enacted a stay-at-home order and a closure of schools, with the intent to limit physical interactions among people and prevent transmission of the virus. Concern arose among patients and their parents that visiting a hospital or doctor's office put them at increased risk for contracting COVID-19, resulting in deferral of many in-person well-child and routine follow-up care visits.4 , 5 For all these reasons, many health care systems, including CHOP, adopted video telemedicine (VTM).6

Asthma is one of the most common chronic childhood diseases, affecting 1 of 12 school-age children in the United States,7 with a higher prevalence in Philadelphia than the national mean.8 , 9 Pollution and respiratory virus exposure, in particular rhinovirus (RV),10 , 11 can worsen asthma symptoms and trigger exacerbations.12 For example, exposure to US Environmental Protection Agency (EPA) criteria air pollutants, including particulate matter less than 2.5 microns (PM2.5), particulate matter less than 10 microns (PM10), ozone, and nitrogen dioxide (NO2), has been associated with increased asthma exacerbations13, 14, 15, 16 and increased risk of developing asthma.17 Viral respiratory infections are also associated with most pediatric asthma exacerbations,18 and people with asthma experience more severe, longer-lasting respiratory viral infections than people without asthma.19 Based on these findings, it was thought that people with asthma were at risk for worse COVID-19 outcomes,20 , 21 although subsequent observational studies have found mixed results in support of this hypothesis.22, 23, 24

The public health interventions adopted to slow down the transmission of SARS-CoV-2 have altered environmental exposure profiles, which also influence the risk of asthma exacerbations. Infection prevention measures, including wearing face masks, washing hands frequently, and social distancing as a result of stay-at-home orders and school closures, reduce person-to-person transmission of all respiratory viruses. The decrease in transportation and industrial activity resulting from COVID-19 restrictions has reduced the emission of primary air pollutants worldwide,25 , 26 and there is current interest in determining the extent to which these changes have affected asthma symptoms.27 In this study, we sought to describe the impact of COVID-19 public health measures on pediatric asthma-related health care utilization, respiratory virus testing in our emergency department (ED), and pollution levels in the greater Philadelphia area.

Methods

Study population

We extracted asthma patient encounter data corresponding to the time period January 17 to May 17 for the years 2015 to 2020 from the CHOP Care Network, which consists of 48 outpatient primary and specialty care clinical sites, 4 urgent care sites, 15 community hospital alliances, and a 557-bed quaternary care center in the greater Philadelphia area. Data from this network have previously been validated as a tool to assess regional disease trends.8 , 28 Asthma diagnosis was established on the basis of encounters having an International Classification of Diseases, Tenth Revision code J45.nn. Accuracy of this definition was confirmed via manual review of 100 patient charts.

Variable selection

For each encounter, its type (ie, inpatient, ED, outpatient, telephone, and VTM) and date were extracted, along with data on the patient's sex, race, ethnicity, date of birth, and payer type. Race was based on self- or parent/guardian selection of 1 of the following categories: “white,” “black,” “Asian or Pacific Islander,” or “Other.” Subjects without a race selection were coded as “Unknown.” Codified asthma-related drug prescription data for all outpatient asthma-related prescriptions, and for outpatient and inpatient systemic steroid prescriptions, were obtained from CHOP provider prescription records (see Table E1 in this article's Online Repository at www.jaci-inpractice.org).

Virology data

CHOP ED results for respiratory viral testing for adenovirus, influenza A virus (IFV-A), influenza B virus (IFV-B), parainfluenza 1, parainfluenza 2, parainfluenza 3, non–COVID-19 coronavirus, metapneumovirus, respiratory syncytial virus (RSV), RV, and COVID-19 via PCR testing were extracted from CHOP's Respiratory Virus Prevalence database. Data for the number of positive test results and tests administered for each virus for the time period January 17 to May 17 during the years 2015 to 2020 were obtained. The number of positive test results for each virus was compared with (1) the total number of tests administered for that virus only and (2) the overall number of viral tests administered for all the viruses listed above.

Air pollution data

Hourly PM2.5, PM10, ozone, and NO2 measures obtained at EPA monitoring sites in Philadelphia for the time period January 17 to May 17 during the years 2015 to 2020 were extracted from AirNow, an air quality data management system that reports real-time and forecast air quality estimates.29 Because historical data were not available for all pollutants in AirNow, we also downloaded daily summary files for the time period January 17 to May 17 during the years 2015 to 2019 from Air Data, an EPA resource that provides quality-assured summary air pollution measures collected from outdoor regulatory monitors across the United States.30 In Philadelphia, the same monitoring sites transmitted data to AirNow and AirData.

Data analysis

Characteristics of encounters, viral test results, and pollutant levels from the 60-day period before and after March 17, 2020 were compared with those from the period 2015 to 2019. A paired Student t test was used to examine differences in systemic steroid prescription rates between patients before and after March 17. For both viral testing and pollution data, controlled interrupted time series regression models were created to identify statistically significant changes between the pre–and post–March 17 60-day time frames that differed in 2020 compared with the 2015 to 2019 historical time period. Significant differences between 2020 and historical data were determined on the basis of P values for regression coefficients corresponding to interaction terms of variables representing pre–and post–March 17 status, the year(s) in question, and/or days. For viral testing, 2-way ANOVA and mixed-effect analysis were additionally used to test for significant differences. To visualize pollution levels across Philadelphia during time periods of interest, we generated 100 m × 100 m grid raster layers using inverse-distance-squared weighted averaging of pollutant measures from the 5 nearest monitoring stations. Analyses were performed in GraphPad Prism (GraphPad Software, San Diego, Calif) and R (R Foundation, Vienna, Austria).31 Results were summarized as percentage change.

Data availability

The epidemiologic data sets supporting the conclusions of this article are available in the Zenodo repository (https://zenodo.org/record/3981568).

Ethical and regulatory oversight

The CHOP Institutional Review Board reviewed our study and determined it did not meet the definition of Human Subjects research.

Results

Asthma health care utilization decreased and VTM encounters increased after COVID-19 public health interventions

Before the public health measures enacted on March 17, 2020 in Philadelphia to limit COVID-19 spread, asthma health care visit numbers and encounter types at CHOP were similar to historical averages for the period 2015 to 2019. Overall, there was a 60% decrease in total daily asthma health care visits at CHOP when comparing the 60 days before and after March 17, 2020 (102.44 ± 48.9; range, 19-190, and 41.5 ± 25.7, range, 0-94, respectively) (Figure 1 ). Before March 17, 2020, the average numbers of outpatient and hospital (ED + inpatient) daily asthma encounters were 72.5 ± 46.2 (range, 0-154) and 25.7 ± 6.6 (range, 0-41), respectively. After March 17, 2020, the average number of daily outpatient encounters decreased by 87% to 9.2 ± 8.2 (range, 0-44), while hospital encounters decreased by 84% to 4.2 ± 3.8 (range, 0-18). Concurrently, asthma telephone encounters across the network increased by 19% from a daily average of 4.3 ± 4.2 (range, 0-24) to 5.1 ± 5.3 (range, 0-21) after March 17, 2020. VTM was not available before March 17, 2020, but was quickly adopted: asthma VTM encounters averaged 23.0 ± 19.9 per day (range, 0-70) and accounted for 61% of all encounters after March 17, 2020.

Figure 1.

Figure 1

Asthma encounters before and after public health interventions were enacted. (A) Daily asthma encounters from January 17 to May 17, 2020. Outpatient (primary + specialty care), telephone calls (telephone), hospital (ED + inpatient), and video (primary + specialty care) encounters are shown. Five-year historical averages (March 18 to May 17, 2015-2019) with 1 SD from the mean for outpatient (light green) or hospital (light purple) encounters shown. March 17 (black-dotted line) is the date Philadelphia prohibited the operation of nonessential businesses (effective 5 PM), and the date the first COVID-19 case was diagnosed at CHOP. (B) Historical and 2020 asthma encounters as a percentage of total. NA, Not applicable/available.

Demographic differences in asthma health care utilization and adoption of VTM

Per-patient demographic characteristics of our study population are presented in Table I . Although the total number of asthma encounters decreased after March 17, 2020, black patients represented a higher proportion of outpatient, hospital, or telephone care after this date compared with the preceding 60-day time period (54% vs 35%, 78% vs 65%, and 49% vs 24%, respectively). Patients with Medicaid coverage represented a higher proportion of outpatient or hospital care after March 17 compared with the pre–March 17, 2020 time period (55% vs 41% and 73% vs 63%, respectively). Of patients who engaged in VTM encounters in the post–March 17, 2020, time period, 26% were black and 30% had Medicaid coverage.

Table I.

Demographic characteristics of subjects with asthma by time period and encounter type

Characteristic Cohort (n)
2015-2019
January 17-March 17, 2020 (5,190)
March 18-May 17, 2020 (2,273)
All (23,146) Outpatient Hospital Telephone Video All Outpatient Hospital Telephone Video All
Sex, n (%)
 Male 13,644 (59) 2,275 (59) 826 (58) 155 (62) 0 (0) 3,035 (58) 253 (56) 122 (50) 169 (57) 808 (59) 1,294 (57)
 Female 9,502 (41) 1,608 (41) 603 (42) 97 (38) 0 (0) 2,155 (42) 196 (44) 124 (50) 129 (43) 573 (41) 979 (43)
Race, n (%)
 White 9,536 (41) 1,711 (44) 251 (18) 151 (60) 0 (0) 2,007 (39) 131 (29) 31 (13) 103 (35) 747 (54) 979 (43)
 Black 9,678 (42) 1,366 (35) 927 (65) 60 (24) 0 (0) 2,139 (41) 242 (54) 191 (78) 145 (49) 356 (26) 880 (39)
 Asian/Pacific Islander 731 (3) 168 (4) 45 (3) 6 (2) 0 (0) 204 (4) 10 (2) 3 (1) 8 (3) 37 (3) 57 (3)
 Other 3,109 (13) 606 (16) 203 (14) 34 (13) 0 (0) 805 (16) 64 (14) 21 (9) 42 (14) 234 (17) 348 (15)
 Unknown 92 (0) 32 (1) 3 (0) 1 (0) 0 (0) 35 (1) 2 (0) 0 (0) 0 (0) 7 (1) 9 (0)
Ethnicity, n (%)
 Non-Hispanic/Latino 20,997 (91) 3,426 (88) 1,274 (89) 223 (88) 0 (0) 4,579 (88) 398 (89) 228 (93) 268 (90) 1,217 (88) 2,018 (89)
 Hispanic/Latino 1,974 (9) 419 (11) 152 (11) 27 (11) 0 (0) 568 (11) 50 (11) 18 (7) 27 (9) 149 (11) 237 (10)
 Unknown 175 (1) 38 (1) 3 (0) 2 (1) 0 (0) 43 (1) 1 (0) 0 (0) 3 (1) 15 (1) 18 (1)
Birth year, n (%)
 Before 2000 1,333 (6) 22 (1) 1 (0) 3 (1) 0 (0) 26 (1) 9 (2) 0 (0) 4 (1) 8 (1) 20 (1)
 2000-2004 4,096 (18) 414 (11) 124 (9) 45 (18) 0 (0) 554 (11) 68 (15) 35 (14) 64 (21) 144 (10) 295 (13)
 2005-2009 6,973 (30) 979 (25) 268 (19) 57 (23) 0 (0) 1,231 (24) 130 (29) 52 (21) 62 (21) 312 (23) 532 (23)
 2010-2014 8,057 (35) 1,343 (35) 492 (34) 89 (35) 0 (0) 1,784 (34) 141 (31) 82 (33) 91 (31) 473 (34) 753 (33)
 2015 or later 2,687 (12) 1,125 (29) 544 (38) 58 (23) 0 (0) 1,595 (31) 101 (22) 77 (31) 77 (26) 444 (32) 673 (30)
Payer type, n (%)
 Non-Medicaid 13,676 (59) 2,283 (59) 532 (37) 222 (88) 0 (0) 2,863 (55) 201 (45) 66 (27) 254 (85) 969 (70) 1,446 (64)
 Medicaid 9,470 (41) 1,600 (41) 897 (63) 30 (12) 0 (0) 2,327 (45) 248 (55) 180 (73) 44 (15) 412 (30) 827 (36)

Decreased prescriptions of systemic steroids after COVID-19 public health interventions

Comparison of pre–and post–March 17, 2020 CHOP prescription patterns found that the relative proportions of most outpatient asthma-related prescriptions were similar before and after introduction of COVID-19 public health interventions (Figure 2 , A). One exception was outpatient systemic steroid prescriptions, which were proportionally reduced compared with other asthma-related medications after the introduction of COVID-19 public health interventions (Figure 2, A). When limiting the comparison to patients who had at least 1 systemic steroid prescription from any primary asthma encounter (outpatient, emergency, or inpatient) between January 17 and May 17, 2020, there was a 83% decrease in systemic steroid prescriptions (Figure 2, B). Black patients and patients with Medicaid coverage represented the highest proportion of steroid prescription encounters between March 17 and May 17, 2020 (70% and 63%, respectively) (see Table E2 in this article's Online Repository at www.jaci-inpractice.org).

Figure 2.

Figure 2

Asthma prescriptions before and after public health interventions were enacted. (A) Outpatient asthma-related prescriptions by medication class as a percentage of total (AC, anticholinergic; β2A, β2 agonists; Bio, biologic; ICS, inhaled corticosteroid; ICS + LABA, ICS with long-acting beta-agonist; LM, leukotriene modifier; Rxs, prescriptions; SS, systemic steroid). (B) Average number of systemic steroid prescriptions per patient per 30 days from any primary asthma encounter (outpatient, emergency, inpatient). Mean + SEM shown. Statistical comparison by paired Student t test. ∗∗∗∗P < .0001.

Decreased RV infections after COVID-19 public health interventions

Given the importance of respiratory viral infections in asthma exacerbations, we sought to quantify the impact of COVID-19 public health interventions on respiratory viral testing. We focused on 4 key viruses; IFV-A, IFV-B, RSV, and RV. When examining viral data for the period 2019 to 2020, we noted variations in season onset and peak timing compared with historical trends. The IFV-A viral season had variable timing year-to-year and had neither an early nor a late season in the period 2019 to 2020 (Figure 3 , A). The IFV-B viral season had an earlier onset and peaked earlier in the period 2019 to 2020, as compared with recent previous years (Figure 3, B). Both the IFV-A and IFV-B seasons were waning by March 17, 2020. The RSV and RV seasonal patterns were similar in all years considered before March 17 (Figure 3, C and D). RSV was waning by March 17, 2020 (Figure 3, C), whereas the 2020 RV season was near its peak on March 17, 2020 (Figure 3, D). Controlled interrupted time series results found some significant changes when comparing 2020 data to previous years' data for all 3 of the 4 viruses (not for INF-A), though year-to-year variability was observed, consistent with variable timing of viral seasons (see Figure E1 in this article's Online Repository at www.jaci-inpractice.org). For example, significant differences were identified for RSV in the period before March 17 though some previous years had higher rates of positive testing than in 2020, whereas others had lower (Figure E1, C, and Table II ). RV was the only virus with significantly decreased levels in the post–March 17, 2020, time period as compared with the same time period during previous years, when years were compared individually or as a 2015 to 2019 historical average (Figure E1, D, and Figure 3, E-G).

Figure 3.

Figure 3

Changes in viral respiratory testing during the COVID-19 pandemic. Deidentified institutional ED virology testing results for the period 2015 to 2020 were accessed. (A-D) Time series plots comparing historical data (2015-2019) to the current year (2020) for rates of positive IFV-A (A), IFV-B (B), RV (C), and RSV (D) testing vs total tests for each virus. (E) For 2020, RV testing data from January 17 to March 17 and March 18 to May 17 were compared to averaged historical data from the same dates from 2015 to 2019. (F) Bar plots comparing the 2 time periods (January 17 to March 17 and March 18 to May 17) from the averaged historical time period (2015-2019) vs the current year (2020). (G) ITS plots comparing time series in 2018, 2019, and 2015 to 2019 averaged vs 2020. For each, the historical data are plotted in a lighter color. The dashed line after week 9 (March 17) is the predicted data based on the previous results, and the uninterrupted line is the actual data from 2020 (exact data also plotted as circles). Significance testing via ANOVA (F) and details in Table II for Figure 3, G. ITS, Interrupted time series.

Figure E1.

Figure E1

Effects of public health interventions designed to limit viral transmission on viral testing. Deidentified institutional ED virology testing results for the period 2015 to 2020 were accessed. (A-D) Bar plots of rates of positive viral testing (IFV-A, IFV-B, RSV, and RV, respectively) from January 17 to March 17 vs March 18 to May 17 in the period 2015 to 2019 (and the average of that range) vs 2020.

Table II.

ITS analysis of viral testing data from CHOP before and after COVID-19 public health interventions were enacted

Years compared IFV-A IFV-B RV RSV
2015 vs 2020 0.93 (NS) 0.025 0.0040 0.016
2016 vs 2020 0.52 (NS) 0.0007 0.021 0.0008
2017 vs 2020 0.59 (NS) 0.014 0.0006 0.0290
2018 vs 2020 0.89 (NS) 0.037 0.0035 0.023
2019 vs 2020 0.81 (NS) 0.011 0.011 0.0057
2015-2019 vs 2020 0.79 (NS) 2.5 × 10−06 0.0074 0.14 (NS)

ITS, Interrupted time series; NS, not significant.

P ≤ .05.

P ≤ .01.

P ≤ .001.

Levels of 4 criteria air pollutants in Philadelphia did not significantly change during the COVID-19 pandemic compared with historical data

Comparison of pre–and post–March 17, 2020 pollution levels (Table III ; Figure 4 , A) found that the daily average of PM2.5, PM10, and NO2 levels decreased by 29.0% (2.17 μg/m3), 18.2% (3.13 μg/m3), and 44.1% (6.75 ppb), respectively, whereas ozone levels increased by 43.4% (10.08 ppb). Historical data for the period 2015 to 2019 showed comparable changes pre–and post–Mar 17: AirNow estimates found that PM2.5 levels decreased by 34.2% (3.88 μg/m3) and ozone increased by 52.4% (10.9 ppb); AirData estimates found that PM2.5 levels decreased by 29.2% (3.15 μg/m3), PM10 by 11.6% (2.63 μg/m3), and NO2 by 28.5% (5.49 ppb), whereas ozone increased by 46.4% (10.69 ppb). Although some of these changes differed significantly across the full range of days (January 17 to May 17), year, and/or before and after the March 17 date, none of the changes were statistically significant compared with historical trends observed across the pre–and post–March 17 60-day time period (see Table E3 in this article's Online Repository at www.jaci-inpractice.org). Specifically, PM2.5 and PM10 had significantly decreased levels in 2020 compared with previous years during the days January 17 to May 17; PM2.5 significantly decreased after March 17 in all years whether using AirNow or AirData historical data (P < .05); ozone had significantly higher levels after March 17 and across all days whether using AirNow or AirData historical data (P < .001); and NO2 significantly decreased across days (P < .05) with no change before or after March 17 or by year. Figure 4, B, shows the raster of PM2.5 levels in Philadelphia for the 60-day pre–and post–March 17 periods along with the location of air monitoring stations that recorded PM2.5 measures.

Table III.

Mean measures of 4 criteria air pollutants in Philadelphia before and after COVID-19 public health interventions were enacted

Air pollutant AirData (2015-2019)
AirNow (2015-2019)
AirNow (2020)
January 17 to March 17 March 18 to May 17 January 17 to March 17 March 18 to May 17 January 17 to March 17 March 18 to May 17
NO2 (ppb) 19.2 ± 6.8 13.7 ± 4.6 NA NA 15.2 ± 7.6 8.5 ± 3.8
Ozone (ppb) 23.0 ± 6.5 33.7 ± 4.9 20.8 ± 5.8 31.7 ± 3.6 23.2 ± 8.5 33.2 ± 5.2
PM2.5 (μg/m3) 10.7 ± 3.5 7.6 ± 2.5 11.3 ± 2.4 7.4 ± 1.7 7.3 ± 4.3 5.2 ± 2.2
PM10 (μg/m3) 22.7 ± 3.4 20.1 ± 3.0 NA NA 17.2 ± 7.7 14.0 ± 4.7

NA, Not available; ppb, parts per billion.

Values are mean ± SD.

Figure 4.

Figure 4

Levels of 4 criteria air pollutants in Philadelphia before and after COVID-19 public health interventions were enacted. (A) Boxplots of averages of daily NO2, ozone, PM10, and PM2.5 measures corresponding to years 2020 and 2015 to 2019 sourced from AirData and AirNow for the 60-day time period before and after March 17, the day in 2020 when COVID-19 public health interventions were enacted in Philadelphia. None of the changes across March 17 were significantly different in the year 2020 compared with historical years. (B) Philadelphia raster layer maps showing daily average PM2.5 levels before and after the COVID-19 public health interventions were enacted for the year 2020 and the average of years 2015 to 2019 using AirNow data. The blue circles denote available air monitoring sites. ppb, Parts per billion.

Discussion

We found that public health interventions designed to limit SARS-CoV-2 transmission in the Philadelphia region were associated with increased VTM and decreased overall asthma encounters, systemic steroid prescriptions, and RV positivity in our ED (Figure 5 ). We previously noted an overall decrease in ED utilization at CHOP,32 a pattern consistent with that observed in other regions of the country, which included a shift away from in-person care and toward VTM-based care.33 Our observed decrease in the overall asthma disease burden is also consistent with national survey data.33

Figure 5.

Figure 5

Effects of public health interventions designed to limit viral transmission on asthma features. Public health interventions designed to limit viral transmission (masking, social distancing, school closures, etc) were associated with a restructuring of asthma care delivery including a reduction in in-person encounters and an increase in VTM-based care. Overall asthma encounters were reduced, as were systemic steroid prescriptions. Changes in RV infections, but not pollution levels, may have contributed to these trends.

After March 17, 2020, VTM became the most used asthma encounter modality at CHOP, enabling patients with asthma to access care while adhering to stay-at-home guidelines. Previous studies have demonstrated the utility of VTM to facilitate care delivery to underserved rural populations and as a viable substitute for both routine and acute in-person asthma care visits.34 , 35 However, the rapid introduction of VTM across the country represents a new, and as such, understudied care model. Black children accounted for the majority of outpatient and hospital care after March 17, 2020, yet they represented only 26% of VTM encounters. We were unable to determine whether this observed difference by race in VTM care was due to patient preference, differences in access to VTM, or some other factor. Future studies should consider this issue carefully in light of well-known disparities in asthma prevalence, severity, and exacerbations by race, ethnicity, and socioeconomic status in the United States,36, 37, 38 as well as concern for a potential “digital divide” in telemedicine.39, 40, 41

Changes in respiratory virus infection rates may have contributed to the decrease in asthma encounters we observed. Most notably, we found that cases of positive RV testing decreased after the introduction of public health interventions designed to limit viral transmission of SARS-CoV-2. This is relevant because RV is a key cause of asthma exacerbations.10 , 11 The other 3 viruses examined (IFV-A, IFV-B, RSV) were waning by March 17, 2020, and as such likely did not play as active a role in asthma exacerbations that occurred after this date. However, we note that we were limited when comparing viral data trends across years because of variability in seasonal onset and peak timing. This variability led to mixed results on the impact of COVID-19 public health interventions on RSV. Overall, a clinically impactful effect of COVID-19–related public health interventions on RSV was unlikely, although the decrease in RV may have contributed to a decrease in asthma exacerbations after March 17.

Air pollution levels are known to vary according to season: PM2.5 and PM10 concentrations across the United States are relatively higher in summer and lower in winter,42 whereas ground-level ozone and NO2 are inversely related, with levels peaking in summer and winter, respectively.43 Our results for each of these 4 criteria air pollutants across the January 17 to May 17 time frame in Philadelphia are consistent with known seasonal trends. Although we did not observe statistically significant changes after COVID-19 public health interventions for these 4 pollutants, the dramatic reduction in vehicular traffic and some industrial activity likely reduced levels of specific pollutants not captured by EPA regulatory monitors. NO2 and PM10 comparisons were limited because they involved 2 different sources of data: AirNow and AirData. Although the same monitoring sites provided data to these publicly available resources, they differed in that AirData releases quality-assured data, whereas AirNow releases real-time measures. Hence, only AirNow contained 2020 measures, whereas only AirData contained complete historical measures. This limitation would likely not change our conclusions because comparison of PM2.5 and ozone measures derived from AirNow and AirData for the period 2015 to 2019 revealed that they were broadly similar. In addition, controlled interrupted time series results were similar whether AirNow or AirData historical measures were used for these 2 pollutants (Table E2). Our pollution results were also limited because they relied on measures taken at specific monitoring sites that may not have adequately captured differences experienced by individuals across the greater Philadelphia region. In addition to potentially changing levels of outdoor air pollutants, COVID-19–related public health interventions likely influenced pollution exposure profiles of children in other ways, including via decreased commuting and outdoor activity.

An additional factor that may have contributed to the reduced asthma disease burden and health care utilization after COVID-19 public health interventions were introduced is increased implementation of preventative measures. For example, some providers may have purposefully reached out to patients' families to encourage filling controller medication prescriptions as the COVID-19 pandemic began, given initial concern that those with asthma had increased susceptibility to more severe outcomes with SARS-CoV-2 infection. In addition, fear of contracting COVID-19 may have reduced the likelihood of an individual accessing in-person care, as well as increased adherence to controller medications.44 Finally, just as social distancing and increased time spent indoors may have limited patient exposure to viruses and outdoor pollution, these measures may have also decreased exposure to outdoor environmental allergens that are known triggers of pediatric asthma.45 School closures may have additionally resulted in reduced exposure to allergens because school environments can be sources of allergens that increase asthma morbidity.46 , 47

Our study is subject to additional limitations worth noting. The demographic, health care utilization, and viral testing data were derived from a single institution and collected as part of routine care. Therefore, our results may not generalize to other regions and are observational in nature. We relied on primary International Classification of Diseases codes to identify asthma encounters, which may be affected by billing or administrative constraints, and hence may have introduced bias in our data collection. Our prescription data are incomplete in that patients may have sought care outside of our network, and it is limited in that we do not have information on prescriptions filled or adherence. Furthermore, we observed an increase in steroid prescriptions in 2020 as compared with previous years. This increase could be due to shifts in patient acuity, or provider prescription practices. Finally, use of electronic health record–derived data is subject to bias and error more broadly, which we were unable to control for, although most errors in the data would have biased us toward not observing significant changes. As such, future studies are warranted to refine our findings and improve our understanding of the effects of the COVID-19 pandemic on asthma care, triggers, and clinical outcomes.

Acknowledgments

We thank Rebecca A. Hubbard, PhD, for statistical advice. Figure 5 was created with BioRender.

Footnotes

This work was supported by the National Institutes of Health (grant no. K08DK116668 to D.A.H.; grant nos. R01HL133433 and R01HL141992 to B.E.H.; grant nos. P30ES013508 and K08AI135091 to S.E.H.; grant no. K23HL136842 to C.C.K.; and grant no. R25HL084665 to K.T.), the American College of Allergy Asthma and Immunology (D.A.H.), the American Academy of Allergy Asthma and Immunology (D.A.H.), the American Partnership for Eosinophilic Disorders (D.A.H.), the Burroughs Wellcome Fund (S.E.H.), and Children’s Hospital of Philadelphia Research Institute Developmental Awards (D.A.H. and S.E.H.). The content of this work is the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Conflicts of interest: S. E. Henrickson has served on prior ad hoc advisory boards for Horizon Pharma, unrelated to this study. The rest of the authors declare that they have no relevant conflicts of interest.

Online Repository.

Table E1.

Asthma medication classes

Medicine ID no. Name Class
61180 Decadron IJ Systemic steroid
61181 Decadron IV Systemic steroid
61183 Decadron OR Systemic steroid
132559 DEX Combo 8-4 mg/mL IJ SUSP Systemic steroid
132710 DEX Combo IJ Systemic steroid
132560 DEX LA 16 16 mg/mL IJ SUSP Systemic steroid
132711 DEX LA 16 IJ Systemic steroid
132561 DEX LA 8 8 mg/mL IJ SUSP Systemic steroid
132712 DEX LA 8 IJ Systemic steroid
130359 Dexameth SOD PHOS-BUPIV-LIDO Systemic steroid
90302 Dexamethasone (glucocorticosteroids) Systemic steroid
61547 Dexamethasone (PAK) OR Systemic steroid
200200162 Dexamethasone 0.1 mg/mL (D5W) injection custom Systemic steroid
200200163 Dexamethasone 0.1 mg/mL (NSS) injection custom Systemic steroid
2762 Dexamethasone 0.5 mg OR TABS Systemic steroid
200200499 Dexamethasone 0.5 mg OR TABS (CHEMO) Systemic steroid
2759 Dexamethasone 0.5 mg/5 mL OR ELIX Systemic steroid
2760 Dexamethasone 0.5 mg/5 mL OR SOLN Systemic steroid
2763 Dexamethasone 0.75 mg OR TABS Systemic steroid
2764 Dexamethasone 1 mg OR TABS Systemic steroid
200201009 Dexamethasone 1 mg OR TABS (CHEMO) Systemic steroid
200200164 Dexamethasone 1 mg/mL (D5W) injection custom Systemic steroid
200200874 Dexamethasone 1 mg/mL (NSS) injection custom Systemic steroid
21292 Dexamethasone 1 mg/mL OR CONC Systemic steroid
200200501 Dexamethasone 1 mg/mL OR CONC (CHEMO) Systemic steroid
135377 Dexamethasone 1.5 mg (21) OR TBPK Systemic steroid
135378 Dexamethasone 1.5 mg (35) OR TBPK Systemic steroid
135379 Dexamethasone 1.5 mg (51) OR TBPK Systemic steroid
2765 Dexamethasone 1.5 mg OR TABS Systemic steroid
200200502 Dexamethasone 1.5 mg OR TABS (CHEMO) Systemic steroid
2766 Dexamethasone 2 mg OR TABS Systemic steroid
200201008 Dexamethasone 2 mg OR TABS (CHEMO) Systemic steroid
2767 Dexamethasone 4 mg OR TABS Systemic steroid
200200503 Dexamethasone 4 mg OR TABS (CHEMO) Systemic steroid
200200504 Dexamethasone 4 mg/mL (undiluted) injection (CHEMO) custom Systemic steroid
200200165 Dexamethasone 4 mg/mL (undiluted) injection custom Systemic steroid
2768 Dexamethasone 6 mg OR TABS Systemic steroid
200200505 Dexamethasone 6 mg OR TABS (CHEMO) Systemic steroid
132777 Dexamethasone ACE & SOD PHOS Systemic steroid
132551 Dexamethasone ACE & SOD PHOS 8-4 mg/mL IJ SUSP Systemic steroid
132713 Dexamethasone ACE & SOD PHOS IJ Systemic steroid
90303 Dexamethasone acetate Systemic steroid
29197 Dexamethasone acetate 16 mg/mL IJ SUSP Systemic steroid
2769 Dexamethasone acetate 8 mg/mL IJ SUSP Systemic steroid
61549 Dexamethasone acetate IJ Systemic steroid
2770 Dexamethasone acetate POWD Systemic steroid
27267 Dexamethasone base POWD Systemic steroid
200200166 Dexamethasone injection custom orderable Systemic steroid
200200506 Dexamethasone injection custom orderable (CHEMO) Systemic steroid
2758 Dexamethasone Intensol 1 mg/mL OR CONC Systemic steroid
61551 Dexamethasone Intensol OR Systemic steroid
61554 Dexamethasone OR Systemic steroid
18270 Dexamethasone POWD Systemic steroid
130355 Dexamethasone SOD PHOS & BUPIV Systemic steroid
130356 Dexamethasone SOD PHOS-LIDO Systemic steroid
121371 Dexamethasone SOD Phosphate PF 10 mg/mL IJ SOLN Systemic steroid
121730 Dexamethasone SOD Phosphate PF IJ Systemic steroid
200201236 Dexamethasone sodium phosphate (CHEMO) 4 mg/mL IJ SOLN Systemic steroid
90304 Dexamethasone sodium phosphate (glucocorticosteroids) Systemic steroid
2771 Dexamethasone sodium phosphate 10 mg/mL IJ SOLN Systemic steroid
200201160 Dexamethasone sodium phosphate 10 mg/mL IJ SOLN (CHEMO) Systemic steroid
128185 Dexamethasone sodium phosphate 100 mg/10 mL IJ SOLN Systemic steroid
128184 Dexamethasone sodium phosphate 120 mg/30 mL IJ SOLN Systemic steroid
128183 Dexamethasone sodium phosphate 20 mg/5 mL IJ SOLN Systemic steroid
2772 Dexamethasone sodium phosphate 4 mg/mL IJ SOLN Systemic steroid
200201065 Dexamethasone sodium phosphate 4 mg/mL INH SOLN custom Systemic steroid
61557 Dexamethasone sodium phosphate IJ Systemic steroid
61558 Dexamethasone sodium phosphate IV Systemic steroid
2776 Dexamethasone sodium phosphate POWD Systemic steroid
135753 DEXPAK 10 DAY 1.5 mg (35) OR TBPK Systemic steroid
97925 DEXPAK 10 DAY OR Systemic steroid
135749 DEXPAK 13 DAY 1.5 mg (51) OR TBPK Systemic steroid
61586 DEXPAK 13 DAY OR Systemic steroid
135755 DEXPAK 6 DAY 1.5 mg (21) OR TBPK Systemic steroid
100127 DEXPAK 6 DAY OR Systemic steroid
130145 Doubledex 10 mg/mL IJ KIT Systemic steroid
130264 Doubledex IJ Systemic steroid
70802 Medrol (PAK) OR Systemic steroid
17892 Medrol 16 mg OR TABS Systemic steroid
5790 Medrol 2 mg OR TABS Systemic steroid
5792 Medrol 32 mg OR TABS Systemic steroid
17891 Medrol 4 mg OR TABS Systemic steroid
135742 Medrol 4 mg OR TBPK Systemic steroid
5793 Medrol 8 mg OR TABS Systemic steroid
70803 Medrol OR Systemic steroid
71141 Methylpred 40 IJ Systemic steroid
130360 Methylprednisol & BUPIV & LIDO Systemic steroid
90309 Methylprednisolone Systemic steroid
128079 Methylprednisolone & lidocaine IJ Systemic steroid
200200507 Methylprednisolone (CHEMO) injection custom orderable Systemic steroid
71143 Methylprednisolone (PAK) OR Systemic steroid
5957 Methylprednisolone 16 mg OR TABS Systemic steroid
12408 Methylprednisolone 2 mg OR TABS Systemic steroid
12410 Methylprednisolone 32 mg OR TABS Systemic steroid
5958 Methylprednisolone 4 mg OR TABS Systemic steroid
135372 Methylprednisolone 4 mg OR TBPK Systemic steroid
12411 Methylprednisolone 8 mg OR TABS Systemic steroid
128116 Methylprednisolone ACE-LIDO Systemic steroid
132562 Methylprednisolone ACE-LIDO 40-10 mg/mL IJ SUSP Systemic steroid
132542 Methylprednisolone ACE-LIDO 80-10 mg/mL IJ SUSP Systemic steroid
132732 Methylprednisolone ACE-LIDO IJ Systemic steroid
90310 Methylprednisolone acetate Systemic steroid
132539 Methylprednisolone acetate 100 mg/mL IJ SUSP Systemic steroid
5959 Methylprednisolone acetate 20 mg/mL IJ SUSP Systemic steroid
5959 Methylprednisolone acetate 40 mg/mL IJ SUSP Systemic steroid
200201903 Methylprednisolone acetate 40 mg/mL IJ SUSP (IR use only) C Systemic steroid
5961 Methylprednisolone acetate 80 mg/mL IJ SUSP Systemic steroid
71145 Methylprednisolone acetate IJ Systemic steroid
121372 Methylprednisolone acetate PF 40 mg/mL IJ SUSP Systemic steroid
121373 Methylprednisolone acetate PF 80 mg/mL IJ SUSP Systemic steroid
121778 Methylprednisolone acetate PF IJ Systemic steroid
20399 Methylprednisolone acetate POWD Systemic steroid
200200293 Methylprednisolone injection custom orderable Systemic steroid
71147 Methylprednisolone OR Systemic steroid
20398 Methylprednisolone POWD Systemic steroid
200200508 Methylprednisolone sodium Succ (CHEMO) 1 mg/mL (NSS) INJECT Systemic steroid
200200509 Methylprednisolone sodium Succ (CHEMO) 1000 mg IJ SOLR Systemic steroid
200200510 Methylprednisolone sodium Succ (CHEMO) 125 mg IJ SOLR Systemic steroid
200201004 Methylprednisolone sodium Succ (CHEMO) 125 mg/mL (SWFI) INJ Systemic steroid
200200511 Methylprednisolone sodium Succ (CHEMO) 40 mg IJ SOLR Systemic steroid
200201002 Methylprednisolone sodium Succ (CHEMO) 40 mg/mL (SWFI) INJ Systemic steroid
90311 Methylprednisolone sodium Succ (glucocorticosteroids) Systemic steroid
52078 Methylprednisolone sodium Succ 1 g IJ SOLR Systemic steroid
200200294 Methylprednisolone sodium Succ 1 mg/mL (NSS) Injection CUST Systemic steroid
12412 Methylprednisolone sodium Succ 1000 mg IJ SOLR Systemic steroid
12413 Methylprednisolone sodium Succ 125 mg IJ SOLR Systemic steroid
200201001 Methylprednisolone sodium Succ 125 mg/mL (SWFI) Injection C Systemic steroid
12414 Methylprednisolone sodium Succ 2000 mg IJ SOLR Systemic steroid
12415 Methylprednisolone sodium Succ 40 mg IJ SOLR Systemic steroid
200200999 Methylprednisolone sodium SUCC 40 mg/mL (SWFI) injection CU Systemic steroid
12416 Methylprednisolone sodium Succ 500 mg IJ SOLR Systemic steroid
71149 Methylprednisolone sodium Succ IJ Systemic steroid
89026 Millipred 10 mg/5 mL OR SOLN Systemic steroid
97492 Millipred 5 mg OR TABS Systemic steroid
135762 Millipred DP 12-DAY 5 mg (48) OR TBPK Systemic steroid
111603 Millipred DP 12-DAY OR Systemic steroid
135756 Millipred DP 5 MG (21) OR TBPK Systemic steroid
135757 Millipred DP 5 mg (48) OR TBPK Systemic steroid
100265 Millipred DP OR Systemic steroid
89183 Millipred OR Systemic steroid
33929 Orapred 15 mg/5 mL OR SOLN Systemic steroid
51263 Orapred ODT 10 mg OR TBDP Systemic steroid
50493 Orapred ODT 15 mg OR TBDP Systemic steroid
51264 Orapred ODT 30 mg OR TBDP Systemic steroid
73649 Orapred ODT OR Systemic steroid
73650 ORAPRED OR Systemic steroid
97196 Pediapred 6.7 (5 mg prednisolone base) mg/5 mL OR SOLN Systemic steroid
74412 Pediapred OR Systemic steroid
90312 Prednisolone Systemic steroid
100776 Prednisolone 15 mg/5 mL OR SOLN Systemic steroid
13018 Prednisolone 15 mg/5 mL OR SYRP Systemic steroid
135373 Prednisolone 5 mg (21) OR TBPK Systemic steroid
135374 Prednisolone 5 mg (48) OR TBPK Systemic steroid
7711 Prednisolone 5 mg OR TABS Systemic steroid
90313 Prednisolone acetate (glucocorticosteroids) Systemic steroid
108953 Prednisolone acetate 16.7 (15 mg base) mg/5 mL OR SUSP Systemic steroid
75589 Prednisolone acetate IJ Systemic steroid
109427 Prednisolone acetate OR Systemic steroid
7716 Prednisolone acetate POWD Systemic steroid
20923 Prednisolone anhydrous POWD Systemic steroid
75593 Prednisolone OR Systemic steroid
7712 Prednisolone POWD Systemic steroid
75595 Prednisolone SOD phosphate OR Systemic steroid
90314 Prednisolone sodium phosphate (glucocorticosteroids) Systemic steroid
51252 Prednisolone sodium phosphate 10 mg OR TBDP Systemic steroid
89025 Prednisolone sodium phosphate 10 mg/5 mL OR SOLN Systemic steroid
50481 Prednisolone sodium phosphate 15 mg OR TBDP Systemic steroid
200201856 Prednisolone sodium phosphate 15 mg/5 mL (SWISH & SPIT) OR S Systemic steroid
33930 Prednisolone sodium phosphate 15 mg/5 mL OR SOLN Systemic steroid
200200533 Prednisolone sodium phosphate 15 mg/5 mL OR SOLN (CHEMO) Cus Systemic steroid
97477 Prednisolone sodium phosphate 20 mg/5 mL OR SOLN Systemic steroid
121526 Prednisolone sodium phosphate 25 mg/5 mL OR SOLN Systemic steroid
51253 Prednisolone sodium phosphate 30 mg OR TBDP Systemic steroid
96082 Prednisolone sodium phosphate 6.7 (5 mg base) mg/5 mL OR SOLN Systemic steroid
75598 Prednisolone sodium phosphate OR Systemic steroid
20439 Prednisolone sodium phosphate POWD Systemic steroid
90315 Prednisone Systemic steroid
75601 Prednisone (PAK) OR Systemic steroid
200200351 Prednisone 0.5 mg/mL OR SOL custom Systemic steroid
7721 Prednisone 1 mg OR TABS Systemic steroid
200200492 Prednisone 1 mg OR TABS (CHEMO) custom Systemic steroid
120527 Prednisone 1 mg OR TBEC Systemic steroid
135431 Prednisone 10 mg (21) OR TBPK Systemic steroid
135432 Prednisone 10 mg (48) OR TBPK Systemic steroid
7722 Prednisone 10 mg OR TABS Systemic steroid
200200493 Prednisone 10 mg OR TABS (CHEMO) custom Systemic steroid
120528 Prednisone 2 mg OR TBEC Systemic steroid
7723 Prednisone 2.5 mg OR TABS Systemic steroid
200200494 Prednisone 2.5 mg OR TABS (CHEMO) custom Systemic steroid
7724 Prednisone 20 mg OR TABS Systemic steroid
200200495 Prednisone 20 mg OR TABS (CHEMO) custom Systemic steroid
135375 Prednisone 5 mg (21) OR TBPK Systemic steroid
135376 Prednisone 5 mg (48) OR TBPK Systemic steroid
7725 Prednisone 5 mg OR TABS Systemic steroid
200200496 Prednisone 5 mg OR TABS (CHEMO) custom Systemic steroid
120529 Prednisone 5 mg OR TBEC Systemic steroid
7720 Prednisone 5 mg/5 mL OR SOLN Systemic steroid
7718 Prednisone 5 mg/mL OR CONC Systemic steroid
7726 Prednisone 50 mg OR TABS Systemic steroid
22674 Prednisone intensol 5 mg/mL OR CONC Systemic steroid
75602 Prednisone Intensol OR Systemic steroid
75603 Prednisone OR Systemic steroid
7727 Prednisone POWD Systemic steroid
7732 Prelone 15 mg/5 mL OR SYRP Systemic steroid
75620 Prelone OR Systemic steroid
8767 Solu-Medrol 1000 mg IJ SOLR Systemic steroid
8768 Solu-Medrol 125 mg IJ SOLR Systemic steroid
8769 Solu-Medrol 2 g IJ SOLR Systemic steroid
8770 Solu-Medrol 40 mg IJ SOLR Systemic steroid
8771 Solu-Medrol 500 mg IJ SOLR Systemic steroid
79793 Solu-Medrol IJ Systemic steroid
79797 Solurex IJ Systemic steroid
79798 Solurex LA IJ Systemic steroid
80064 Sterapred 12 DAY OR Systemic steroid
80065 Sterapred DS 12 DAY OR Systemic steroid
80066 Sterapred DS OR Systemic steroid
80067 Sterapred OR Systemic steroid
36549 Accuneb 0.63 mg/3 mL IN NEBU Beta-agonist
36550 Accuneb 1.25 mg/3 mL IN NEBU Beta-agonist
53821 Accuneb IN Beta-agonist
54377 Airet IN Beta-agonist
91225 Albuterol Beta-agonist
54543 Albuterol IN Beta-agonist
20261 Albuterol POWD Beta-agonist
91226 Albuterol sulfate Beta-agonist
311 Albuterol sulfate (2.5 mg/3 mL) 0.083% IN NEBU Beta-agonist
312 Albuterol sulfate (5 mg/mL) 0.5% IN NEBU Beta-agonist
200200745 Albuterol sulfate (5 mg/mL) 0.5% NEB continuous custom Beta-agonist
36541 Albuterol sulfate 0.63 mg/3 mL IN NEBU Beta-agonist
36542 Albuterol sulfate 1.25 mg/3 mL IN NEBU Beta-agonist
132129 Albuterol sulfate 108 (90 μg base) μg/ACT IN AEPB Beta-agonist
315 Albuterol sulfate 2 mg OR TABS Beta-agonist
314 Albuterol sulfate 2 mg/5 mL OR SYRP Beta-agonist
316 Albuterol sulfate 4 mg OR TABS Beta-agonist
39219 Albuterol sulfate ER 4 mg OR TB12 Beta-agonist
39220 Albuterol sulfate ER 8 mg OR TB12 Beta-agonist
123418 Albuterol sulfate ER OR Beta-agonist
21155 Albuterol sulfate HFA 108 (90 μg base) μg/ACT IN AERS Beta-agonist
200200995 Albuterol sulfate HFA 108 (90 μg base) μg/ACT IN AERS (ED HOM) Beta-agonist
200200994 Albuterol sulfate HFA 108 (90 μg base) μg/ACT IN AERS (OR Use) Beta-agonist
98773 Albuterol sulfate HFA IN Beta-agonist
54545 Albuterol sulfate IN Beta-agonist
54546 Albuterol sulfate OR Beta-agonist
317 Albuterol sulfate POWD Beta-agonist
2002001992 Albuterol sulfate variable dose for Pyxis Beta-agonist
91234 Levalbuterol HCL (sympathomimetics) Beta-agonist
37337 Levalbuterol HCL 0.31 mg/3 mL IN NEBU Beta-agonist
29159 Levalbuterol HCL 0.63 mg/3 mL IN NEBU Beta-agonist
44604 Levalbuterol HCL 1.25 mg/0.5 mL IN NEBU Beta-agonist
29160 Levalbuterol HCL 1.25 mg/3 mL IN NEBU Beta-agonist
69516 Levalbuterol HCL IN Beta-agonist
91235 Levalbuterol tartrate Beta-agonist
49020 Levalbuterol tartrate 45 μg/ACT IN AERO Beta-agonist
69517 Levalbuterol tartrate IN Beta-agonist
50377 Proair HFA 108 (90 μg base) μg/ACT IN AERS Beta-agonist
75956 Proair HFA IN Beta-agonist
132126 Proair respiclick 108 (90 μg base) μg/ACT IN AEPB Beta-agonist
132374 Proair respiclick IN Beta-agonist
21277 Proventil HFA 108 (90 μg base) μg/ACT IN AERS Beta-agonist
76250 Proventil HFA IN Beta-agonist
76251 Proventil IN Beta-agonist
76252 Proventil OR Beta-agonist
200200406 Terbutaline 0.1% nebulization SOLN custom Beta-agonist
91239 Terbutaline sulfate Beta-agonist
200200937 Terbutaline sulfate 0.1 mg/mL IJ SOLN custom Beta-agonist
13430 Terbutaline sulfate 1 mg/mL IJ SOLN Beta-agonist
200201165 Terbutaline sulfate 1 mg/mL IJ SOLN (subcutaneous use only) Beta-agonist
200200407 Terbutaline sulfate 1 mg/mL SUSP custom Beta-agonist
13432 Terbutaline sulfate 2.5 mg OR TABS Beta-agonist
13433 Terbutaline sulfate 5 mg OR TABS Beta-agonist
81143 Terbutaline sulfate IJ Beta-agonist
200200938 Terbutaline sulfate injection custom orderable Beta-agonist
81144 Terbutaline sulfate OR Beta-agonist
20433 Terbutaline sulfate POWD Beta-agonist
37396 Xopenex 0.31 mg/3 mL IN NEBU Beta-agonist
29270 Xopenex 0.63 mg/3 mL IN NEBU Beta-agonist
29271 Xopenex 1.25 mg/3 mL IN NEBU Beta-agonist
44598 Xopenex concentrate 1.25 mg/0.5 mL IN NEBU Beta-agonist
83997 Xopenex concentrate IN Beta-agonist
49017 Xopenex HFA 45 μg/ACT IN AERO Beta-agonist
83998 Xopenex HFA IN Beta-agonist
83999 Xopenex IN Beta-agonist
54262 Aerobid IN ICS
54263 Aerobid-M IN ICS
127561 Aerospan 80 μg/ACT IN AERS ICS
127718 Aerospan IN ICS
96592 Alvesco 160 μg/ACT IN AERS ICS
96591 Alvesco 80 μg/ACT IN AERS ICS
97729 Alvesco IN ICS
130919 Arnuity Ellipta 100 μg/ACT IN AEPB ICS
130920 Arnuity Ellipta 200 μg/ACT IN AEPB ICS
130972 Arnuity Ellipta IN ICS
47449 Asmanex 120 metered doses 220 μg/INH IN AEPB ICS
55726 Asmanex 120 metered doses IN ICS
47450 Asmanex 14 metered doses 220 μg/INH IN AEPB ICS
55727 Asmanex 14 metered doses IN ICS
89591 Asmanex 30 metered doses 110 μg/INH IN AEPB ICS
47447 Asmanex 30 metered doses 220 μg/INH IN AEPB ICS
55728 Asmanex 30 metered doses IN ICS
47448 Asmanex 60 metered doses 220 μg/INH IN AEPB ICS
55729 Asmanex 60 metered doses IN ICS
111284 Asmanex 7 metered doses 110 μg/INH IN AEPB ICS
111529 Asmanex 7 metered doses IN ICS
130881 Asmanex HFA 100 μg/ACT IN AERO ICS
130893 Asmanex HFA 200 μg/ACT IN AERO ICS
130973 Asmanex HFA IN ICS
56112 Azmacort IN ICS
91254 Beclomethasone dipropionate (steroid inhalants) ICS
33588 Beclomethasone dipropionate 40 μg/ACT IN AERS ICS
33589 Beclomethasone dipropionate 80 μg/ACT IN AERS ICS
56626 Beclomethasone dipropionate IN ICS
56627 Beclovent IN ICS
91255 Budesonide (steroid inhalants) ICS
33341 Budesonide 0.25 mg/2 mL IN SUSP ICS
33342 Budesonide 0.5 mg/2 mL IN SUSP ICS
200201034 Budesonide 0.5 mg/2 mL NEB for po use ICS
85108 Budesonide 1 mg/2 mL IN SUSP ICS
98957 Budesonide 180 μg/ACT IN AEPB ICS
98956 Budesonide 90 μg/ACT IN AEPB ICS
98788 Budesonide IN ICS
98448 Ciclesonide (steroid inhalants) ICS
96103 Ciclesonide 160 μg/ACT IN AERS ICS
96102 Ciclesonide 80 μg/ACT IN AERS ICS
97832 Ciclesonide IN ICS
98924 Flovent Diskus 100 μg/BLIST IN AEPB ICS
98925 Flovent Diskus 250 μg/BLIST IN AEPB ICS
53294 Flovent Diskus 50 μg/BLIST IN AEPB ICS
64815 Flovent Diskus IN ICS
46255 Flovent HFA 110 μg/ACT IN AERO ICS
46256 Flovent HFA 220 μg/ACT IN AERO ICS
46254 Flovent HFA 44 μg/ACT IN AERO ICS
64816 Flovent HFA IN ICS
64817 Flovent IN ICS
64818 Flovent Rotadisk IN ICS
91256 Flunisolide (steroid inhalants) ICS
127699 Flunisolide HFA ICS
127438 Flunisolide HFA 80 μg/ACT IN AERS ICS
127758 Flunisolide HFA IN ICS
64856 Flunisolide IN ICS
20361 Flunisolide POWD ICS
131120 Fluticasone furoate (steroid inhalants) ICS
130716 Fluticasone furoate 100 μg/ACT IN AEPB ICS
130717 Fluticasone furoate 200 μg/ACT IN AEPB ICS
131018 Fluticasone furoate IN ICS
91257 Fluticasone propionate (INHAL) ICS
32750 Fluticasone propionate (INHAL) 100 μg/BLIST IN AEPB ICS
32751 Fluticasone propionate (INHAL) 250 μg/BLIST IN AEPB ICS
32749 Fluticasone propionate (INHAL) 50 μg/BLIST IN AEPB ICS
64934 Fluticasone propionate (INHAL) IN ICS
91258 Fluticasone propionate HFA ICS
46046 Fluticasone propionate HFA 110 μg/ACT IN AERO ICS
46047 Fluticasone propionate HFA 220 μg/ACT IN AERO ICS
46045 Fluticasone propionate HFA 44 μg/ACT IN AERO ICS
134419 Fluticasone propionate HFA IN ICS
91259 Mometasone furoate (steroid inhalants) ICS
130882 Mometasone furoate 100 μg/ACT IN AERO ICS
89590 Mometasone furoate 110 μg/INH IN AEPB ICS
130883 Mometasone furoate 200 μg/ACT IN AERO ICS
47345 Mometasone furoate 220 μg/INH IN AEPB ICS
71565 Mometasone furoate IN ICS
33535 Pulmicort 0.25 mg/2 mL IN SUSP ICS
33536 Pulmicort 0.5 mg/2 mL IN SUSP ICS
85111 Pulmicort 1 mg/2 mL IN SUSP ICS
99899 Pulmicort flexhaler 180 μg/ACT IN AEPB ICS
99900 Pulmicort flexhaler 90 μg/ACT IN AEPB ICS
76405 Pulmicort flexhaler IN ICS
76406 Pulmicort IN ICS
76407 Pulmicort turbuhaler IN ICS
33585 QVAR 40 μg/ACT IN AERS ICS
33586 QVAR 80 μg/ACT IN AERS ICS
76802 QVAR IN ICS
91260 Triamcinolone acetonide (steroid inhalants) ICS
85453 Triamcinolone acetonide IN ICS
83089 Vanceril double strength IN ICS
83090 Vanceril IN ICS
105585 Advair Diskus 100-50 μg/dose IN AEPB ICS + LABA
105588 Advair Diskus 250-50 μg/dose IN AEPB ICS + LABA
105589 Advair Diskus 500-50 μg/dose IN AEPB ICS + LABA
54204 Advair Diskus IN ICS + LABA
50623 Advair HFA 115-21 μg/ACT IN AERO ICS + LABA
50624 Advair HFA 230-21 μg/ACT IN AERO ICS + LABA
50622 Advair HFA 45-21 μg/ACT IN AERO ICS + LABA
54205 Advair HFA IN ICS + LABA
125719 BREO Ellipta 100-25 μg/INH IN AEPB ICS + LABA
132901 BREO Ellipta 200-25 μg/INH IN AEPB ICS + LABA
125944 BREO Ellipta IN ICS + LABA
91246 Budesonide-formoterol fumarate ICS + LABA
53024 Budesonide-formoterol fumarate 160-4.5 μg/ACT IN AERO ICS + LABA
53023 Budesonide-formoterol fumarate 80-4.5 μg/ACT IN AERO ICS + LABA
57629 Budesonide-formoterol fumarate IN ICS + LABA
110610 Dulera 100-5 μg/ACT IN AERO ICS + LABA
110611 Dulera 200-5 μg/ACT IN AERO ICS + LABA
110811 Dulera IN ICS + LABA
126085 Fluticasone furoate-Vilanterol ICS + LABA
125641 Fluticasone furoate-Vilanterol 100-25 μg/INH IN AEPB ICS + LABA
132806 Fluticasone furoate-Vilanterol 200-25 μg/INH IN AEPB ICS + LABA
125999 Fluticasone furoate-Vilanterol IN ICS + LABA
91247 Fluticasone-salmeterol ICS + LABA
105249 Fluticasone-salmeterol 100-50 μg/dose IN AEPB ICS + LABA
50619 Fluticasone-salmeterol 115-21 μg/ACT IN AERO ICS + LABA
50620 Fluticasone-salmeterol 230-21 μg/ACT IN AERO ICS + LABA
105250 Fluticasone-salmeterol 250-50 μg/dose IN AEPB ICS + LABA
50618 Fluticasone-salmeterol 45-21 μg/ACT IN AERO ICS + LABA
105251 Fluticasone-salmeterol 500-50 μg/dose IN AEPB ICS + LABA
64938 Fluticasone-salmeterol IN ICS + LABA
111224 Mometasone furo-formoterol FUM ICS + LABA
110576 Mometasone furo-formoterol FUM 100-5 μg/ACT IN AERO ICS + LABA
110577 Mometasone furo-formoterol FUM 200-5 μg/ACT IN AERO ICS + LABA
110835 Mometasone furo-formoterol FUM IN ICS + LABA
53239 Symbicort 160-4.5 μg/ACT IN AERO ICS + LABA
53238 Symbicort 80-4.5 μg/ACT IN AERO ICS + LABA
80691 Symbicort IN ICS + LABA
128121 Umeclidinium-Vilanterol ICS + LABA
127865 UMeclidinium-Vilanterol 62.5-25 μg/INH IN AEPB ICS + LABA
128105 Umeclidinium-Vilanterol IN ICS + LABA
30756 Accolate 10 mg OR TABS Leukotriene modulators
21303 Accolate 20 mg OR TABS Leukotriene modulators
53764 Accolate OR Leukotriene modulators
91262 Montelukast sodium (leukotriene modulators) Leukotriene modulators
26447 Montelukast sodium 10 mg OR TABS Leukotriene modulators
31645 Montelukast sodium 4 mg OR CHEW Leukotriene modulators
41211 Montelukast sodium 4 mg OR PKT Leukotriene modulators
26448 Montelukast sodium 5 mg OR Chew Leukotriene modulators
71666 Montelukast sodium OR Leukotriene modulators
26454 Singulair 10 mg OR TABS Leukotriene modulators
31649 Singulair 4 mg OR Chew Leukotriene modulators
41210 Singulair 4 mg OR PKT Leukotriene modulators
26451 Singulair 5 mg OR Chew Leukotriene modulators
79047 Singulair OR Leukotriene modulators
91263 Zafirlukast Leukotriene modulators
30767 Zafirlukast 10 mg OR TABS Leukotriene modulators
21309 Zafirlukast 20 mg OR TABS Leukotriene modulators
84136 Zafirlukast OR Leukotriene modulators
91261 Zileuton Leukotriene modulators
22305 Zileuton 600 mg OR TABS Leukotriene modulators
85485 Zileuton ER 600 mg OR TB12 Leukotriene modulators
120894 Zileuton ER OR Leukotriene modulators
84194 Zileuton OR Leukotriene modulators
22304 Zyflo 600 mg OR TABS Leukotriene modulators
85530 Zyflo CR 600 mg OR TB12 Leukotriene modulators
85882 Zyflo CR OR Leukotriene modulators
84345 Zyflo OR Leukotriene modulators
134493 Mepolizumab Biologics
134274 Mepolizumab 100 mg SC SOLR Biologics
134437 Mepolizumab SC Biologics
134298 Nucala 100 mg SC SOLR Biologics
134446 Nucala SC Biologics
91264 Omalizumab Biologics
41330 Omalizumab 150 mg SC SOLR Biologics
73347 Omalizumab SC Biologics
41342 Xolair 150 mg SC SOLR Biologics
83995 Xolair SC Biologics
120900 Aclidinium bromide Anticholinergics
120515 Aclidinium bromide 400 μg/ACT IN AEPB Anticholinergics
120732 Aclidinium bromide IN Anticholinergics
46720 Atrovent HFA 17 μg/ACT IN AERS Anticholinergics
55931 Atrovent HFA IN Anticholinergics
55932 Atrovent IN Anticholinergics
134491 Glycopyrrolate (bronchodilators-anticholinergics) Anticholinergics
134424 Glycopyrrolate IN Anticholinergics
130918 Incruse Ellipta 62.5 μg/INH IN AEPB Anticholinergics
131033 Incruse Ellipta IN Anticholinergics
91220 Ipratropium bromide (bronchodilators- anticholinergics) Anticholinergics
14727 Ipratropium bromide 0.02 % IN SOLN Anticholinergics
91221 Ipratropium bromide HFA Anticholinergics
46527 Ipratropium bromide HFA 17 μg/ACT IN AERS Anticholinergics
68438 Ipratropium bromide HFA IN Anticholinergics
68439 Ipratropium bromide IN Anticholinergics
20367 Ipratropium bromide POWD Anticholinergics
134455 Seebri Neohaler IN Anticholinergics
43683 Spiriva Handihaler 18 μg IN CAPS Anticholinergics
79945 Spiriva Handihaler IN Anticholinergics
133764 Spiriva Respimat 1.25 μg/ACT IN AERS Anticholinergics
130566 Spiriva Respimat 2.5 μg/ACT IN AERS Anticholinergics
130663 Spiriva Respimat IN Anticholinergics
91222 Tiotropium bromide monohydrate Anticholinergics
133714 Tiotropium bromide monohydrate 1.25 μg/ACT IN AERS Anticholinergics
43672 Tiotropium bromide monohydrate 18 μg IN CAPS Anticholinergics
130394 Tiotropium bromide monohydrate 2.5 μg/ACT IN AERS Anticholinergics
81562 Tiotropium bromide monohydrate IN Anticholinergics
120704 Tudorza Pressair 400 μg/ACT IN AEPB Anticholinergics
120880 Tudorza Pressair IN Anticholinergics
131119 Umeclidinium bromide Anticholinergics
130705 Umeclidinium bromide 62.5 μg/INH IN AEPB Anticholinergics
131098 Umeclidinium bromide IN Anticholinergics
91245 Ipratropium-albuterol Anticholinergics
97202 Ipratropium-albuterol 0.5-2.5 (3) mg/3 mL IN SOLN Anticholinergics
16477 Ipratropium-albuterol 18-103 μg/ACT IN AERO Anticholinergics
119838 Ipratropium-albuterol 20-100 μg/ACT IN AERS Anticholinergics
98087 Ipratropium-albuterol IN Anticholinergics

AERO, Aerosolized; AERS, aerosolized; CHEMO, chemotherapy; CONC, concentrate; CUST, custom; D5W, dextrose 5% in water; Dex, dexamethasone; ELIX, elixer; ER, extended-release; HCL, hydrochloride; HFA, hydrofluoroalkane; ICS, inhaled corticosteroid; IJ, injection; IN, inhallation; INH, inhallation; INHAL, inhallation; INJ, injection; INJECT, injection; IV, intravenous; LABA, long-acting beta agonist; LIDO, lidocaine; NEB, nebulizer; NEBU, nebulizer; NSS, normal saline solution; OR, oral; PAK, pack; PHOS, phosphate; PKT, packet; po, per os (by mouth); POWD, powder; SC, subcutaneous; SOD, sodium; SOL, solution; SOLN, solution; SUSP, suspension; SWFI, sterile water for injection; SYRP, syrup; TABS, tablets; TBEC, enteric coated tablet; TBPK, tablet pack.

Table E2.

Demographic characteristics of asthma prescription encounters

Characteristic Prescription cohort (n)
All medicines (1624) Steroids (402)
Sex, n (%)
 Male 917 (56) 213 (53)
 Female 708 (44) 189 (47)
Race, n (%)
 White 664 (41) 74 (18)
 Black 666 (41) 280 (70)
 Asian/Pacific Islander 36 (2) 6 (1)
 Other 252 (16) 42 (10)
 Unknown 7 (0) 0 (0)
Ethnicity, n (%)
 Non-Hispanic/Latino 1434 (88) 372 (93)
 Hispanic/Latino 180 (11) 30 (7)
 Unknown 11 (1) 0 (0)
Birth year, n (%)
 Before 2000 11 (1) 1 (0)
 2000-2004 208 (13) 62 (15)
 2005-2009 392 (24) 85 (21)
 2010-2014 533 (33) 131 (33)
 2015 or later 481 (30) 123 (31)
Payer type, n (%)
 Non-Medicaid 912 (56) 148 (37)
 Medicaid 713 (44) 254 (63)

Table E3.

Controlled interrupted time series regression analysis results for 4 criteria air pollutants

Variables PM2.5
Ozone
PM10
NO2
AirNow AirData AirNow AirData AirData AirData
Days (P value) −0.03 (.064) −0.05 (.002) 0.26 (<.0001) 0.27 (<.0001) −0.044 (.23) −0.07 (.04)
Year 2020 (P value) −3.51 (.0005) −3.58 (.0002) 2.18 (.25) 1.16 (.54) −5.40 (.004) −0.77 (.66)
Covid_restrictions (P value) −5.25 (.009) −4.56 (.019) 16.08 (<.0001) 12.90 (.0007) −0.52 (.88) −0.33 (.92)
Days × Year 2020 (P value) 0.0009 (.97) 0.02 (.41) −0.03 (.52) −0.04 (.42) −0.005 (.92) −0.01 (.70)
Days × Covid_restrictions (P value) 0.045 (.10) 0.05 (.04) −0.24 (<.0001) −0.2 (<.0001) 0.006 (.90) −0.001 (.98)
Year 2020 × Covid_restrictions (P value) 2.24 (.42) 1.56 (.56) −6.56 (.21) −3.48 (.51) −7.57 (.15) −5.5 (.26)
Days × Year 2020 × Covid_restrictions (P value) −0.005 (.88) −0.01 (.66) 0.09 (.2) 0.05 (.44) 0.08 (.27) 0.05 (.41)

Outcome was levels of each pollutant. Independent variables included days, referring to the 120 d between January 17 and May 17; year 2020, indicating whether it was the year 2020 or historical time period; covid_restrictions, indicating whether the measure was from before or after March 17. Each column corresponds to 1 model with indicated outcome variable and source of historical measures (AirNow or AirData). Terms in the model are indicated in each row. Values are coefficient estimate (P value).

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The epidemiologic data sets supporting the conclusions of this article are available in the Zenodo repository (https://zenodo.org/record/3981568).


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